Capsule Summary:
Shellfish allergy affects a substantial proportion of US adults, many of whom develop the disease during adulthood. Crustacean and mollusk allergies have different manifestations including differing symptomatology, geographic distribution, and are often not comorbid.
Keywords: Shellfish allergy; crustacean allergy; epidemiology, mollusk allergy; food allergy; adult-onset allergy
To the editor:
Shellfish allergy (SA) is one of the most common food allergies worldwide1,2 and third most common in US children3. Although the isolation of specific shellfish allergens and immunologic mechanisms has improved understanding of SA pathophysiology4, knowledge gaps remain regarding the prevalence, distribution and determinants of SAs among US adults5. Consequently, this study estimates national SA prevalence, characteristics and severity within a large, nationally-representative sample of 40,443 US adults surveyed between October 2015 and September 2016. Details regarding survey development, complex survey sampling, weighting, statistical methodologies, and outcomes measures for food allergy assessment—including their unique strengths and limitations are detailed in Gupta et al (2019)6.
In short, reported allergies were considered convincingly IgE-mediated if reported symptoms included at least one stringent symptom (eFigure 1) upon ingestion of the responsible allergen. Classification of physician-confirmed and severe allergies is summarized in eFigure 2. For analyses comparing characteristics of crustacean-allergic versus mollusk-allergic adults, individuals reporting both allergies were excluded. Coastal residence was determined at the county level via residential ZIP using National Oceanic and Atmospheric Administration definitions of coastal state, coastal county, and shoreline counties7 not bordering the Great Lakes. Please note that, since ZIP codes were only queried for participants’ current residence, this may lead to inaccurate estimates for respondents who had moved since developing SA.
Population-weighted demographic and atopic disease characteristics are presented in Table 1. Mean age of SA diagnosis was 17.7 (95% CI, 16.6–18.7%) and mean age of adult-onset SA was 28.3 (95% CI, 26.9–29.8%). SA prevalence by allergen types and age categories are presented in eTable 1. Overall, estimated SA prevalence was 2.9% (2.7–3.1%) while physician-confirmed SA prevalence was 1.2% (1.1–1.3%). Among all adults, 2.4% were estimated to be crustacean-allergic, while 1.2% were estimated to have a physician-confirmed crustacean allergy. Additionally, 1.6% were estimated to be mollusk-allergic, with 0.5% estimated as having a physician-confirmed mollusk allergy.
Table 1.
Demographic Characteristics of the Study Population % (95% CI)
| Variable | All Adults | Adults with Convincing Shellfish Allergy | p-value | Adults with Convincing Crustacean Allergy Only (no mollusk allergy) | Adults with Convincing Mollusk Allergy Only (no crustacean allergy) | p- value |
|---|---|---|---|---|---|---|
| Age (y) | ||||||
| 18–29 | 21.5 (20.8–22.1) | 20.5 (17.9–23.4) | 0.51 | 18.2 (15.0–22.0) | 21.1 (13.5–31.5) | .55 |
| 30–39 | 17.0 (16.5–17.5) | 21.0 (18.3–23.9) | .002 | 20.1 (16.3–24.6) | 21.6 (14.5–31.1) | .74 |
| 40–49 | 16.8 (16.3–17.3) | 14.6 (12.5–16.9) | 0.06 | 14.6 (11.6–18.2) | 12.5 (8.0–18.9) | .52 |
| 50–59 | 18.0 (17.5–18.5) | 20.2 (17.7–23.0) | 0.09 | 20.9 (17.1–25.3) | 19.7 (13.9–27.2) | .77 |
| 60+ | 26.8 (26.2–27.4) | 23.8 (20.9–26.9) | .05 | 26.1 (21.7–31.0) | 25.1 (18.3–33.5) | .83 |
| Gender | ||||||
| Female | 51.7 (51.0–52.4) | 65.0 (61.8–68.1) | <.001 | 63.6 (58.7–68.3) | 62.9 (53.4–71.4) | 0.89 |
| Male | 48.3 (47.6–49.0) | 35.0 (31.9–38.2) | 36.4 (31.8–41.3) | 37.1 (28.6–46.6) | ||
| Race/ethnicity | ||||||
| Asian, Non-Hispanic | 3.9 (3.6–4.1) | 5.0 (3.9–6.4) | 0.04 | 5.9 (4.3–8.1) | 5.2 (2.4–11.2) | 0.77 |
| Black, Non-Hispanic | 11.7 (11.3–12.1) | 13.2 (11.2–15.5) | 0.15 | 15.7 (12.5–19.7) | 8.6 (4.8–15.0) | 0.045 |
| White, Non-Hispanic | 64.9 (64.2–65.6) | 57.8 (54.4–61.2) | <.001 | 56.3 (51.2–61.2) | 59.7 (49.8–69.0) | 0.54 |
| Hispanic/Latino | 15.5 (14.9–16.1) | 17.9 (15.3–20.9) | .07 | 15.9 (12.6–19.9) | 16.5 (9.4–27.2) | 0.91 |
| Multiple/Other | 4.1 (3.8–4.4) | 6.1 (4.4–8.4) | 0.02 | 6.1 (3.6–10.3) | 9.9 (5.3–17.9) | 0.24 |
| Household income | ||||||
| <25K | 16.6 (16.2–17.1) | 17.0 (14.6–19.7) | 0.77 | 16.5 (13.5–19.9) | 19.7 (12.1–30.4) | 0.49 |
| 25K-49K | 22.0 (21.4–22.5) | 20.9 (18.5–23.4) | 0.39 | 19.8 (16.4–23.8) | 18.2 (13.1–24.7) | 0.64 |
| 50K-99K | 30.9 (30.3–31.5) | 33.8 (30.8–37.0) | 0.06 | 33.8 (29.3–38.6) | 32.4 (24.6–41.3) | 0.77 |
| 100K-149K | 19.6 (19.0–20.2) | 20.3 (17.4–23.5) | 0.67 | 21.2 (16.8–26.4) | 23.4 (16.0–32.9) | 0.65 |
| 150K+ | 10.9 (10.4–11.5) | 8.1 (6.3–10.3) | 0.01 | 8.7 (6.1–12.4) | 6.3 (3.4–11.6) | 0.37 |
| Proximity of geographic location to the coast | ||||||
| Coastal States | 60.6 (60.0–61.3) | 63.5 (60.3–66.6) | 0.08 | 65.0 (60.3–69.4) | 63.2 (53.9–71.6) | 0.73 |
| Inland States | 39.4 (38.7–40.0) | 36.5 (33.4–39.7) | 35.0 (30.6–39.7) | 36.8 (28.4–46.1) | ||
| Coastal Watershed Counties | 54.2 (53.5–54.8) | 56.5 (53.1–59.8) | 0.17 | 57.3 (52.3–62.1) | 50.6 (41.2–59.9) | .22 |
| Non-Costal Watershed Counties | 45.9 (45.2–46.5) | 43.5 (40.2–46.9) | 42.7 (37.9–47.7) | 49.4 (40.1–58.8) | ||
| Shoreline Counties | 41.3 (40.7–42.0) | 45.4 (42.1–48.8) | .02 | 47.7 (42.7–52.7) | 39.3 (30.7–48.6) | .12 |
| Non-Shoreline Counties | 58.7 (58.0–59.3) | 54.6 (51.2–57.9) | 52.3 (47.3–57.3) | 60.7 (51.4–69.3) | ||
| Age of SA diagnosis (Mean, 95%CI) | N/A | 17.7 (16.6–18.7) | N/A | 18.8 (17.3–20.3) | 21.1 (17.6–24.7) | N/A |
| Age of adult-onset SA diagnosis (Mean, 95%CI) | N/A | 28.3 (26.9–29.8) | N/A | 27.8 (25.6–30.1) | 33.9 (29.6–38.2) | N/A |
| Physician diagnosed comorbidities | ||||||
| Asthma | 12.3 (11.9–12.7) | 23.2 (20.6–26.0) | <.001 | 24.7 (20.7–29.2) | 14.4 (9.6–21.0) | 0.01 |
| Eczema | 6.7 (6.4–7.1) | 11.8 (9.7–14.2) | <.001 | 10.1 (7.4–13.8) | 12.2 (7.3–19.7) | 0.54 |
| Allergic Rhinitis | 21.4 (20.9–22.0) | 33.4 (30.3–36.7) | <.001 | 32.8 (28.2–37.9) | 33.9 (25.9–42.8) | 0.84 |
| Insect sting allergy | 3.8 (3.6–4.1) | 7.6 (6.2–9.4) | <.001 | 7.0 (4.9–9.7) | 7.5 (4.2–12.9) | 0.84 |
| Latex allergy | 2.3 (2.1–2.5) | 5.4 (4.2–6.9) | <.001 | 4.8 (3.0–7.5) | 3.2 (1.5–6.8) | 0.37 |
| Medication allergy | 13.4 (13.0–13.9) | 24.1 (21.2–27.1) | <.001 | 25.9 (21.5–30.9) | 23.7 (17.2–31.9) | 0.63 |
| Urticaria/chronic hives | .9 (.8–1.0) | 2.5 (1.7–3.5) | <.001 | 2.6 (1.5–4.3) | 2.1 (.8–5.5) | 0.73 |
| Family history of allergic diseases | ||||||
| Parental asthma | 13.5 (13.1–14.0) | 22.2 (19.4–25.3) | <.001 | 25.5 (21.0–30.5) | 14.4 (8.9–22.4) | 0.02 |
| Parental eczema | 9.6 (9.2–10.0) | 15.9 (13.4–18.7) | <.001 | 14.2 (11.0–18.1) | 17.3 (10.6–27.0) | 0.47 |
| Parental environmental allergies | 28.7 (28.0–29.4) | 38.6 (35.1–42.2) | <.001 | 38.8 (33.6–44.2) | 40.4 (30.6–51.0) | 0.78 |
| Parental FA | 12.9 (12.4–13.4) | 37.1 (33.5–40.9) | <.001 | 34.3 (29.2–39.9) | 43.3 (32.8–54.6) | 0.14 |
| Sibling(s) with FA | 16.6 (16.1–17.2) | 33.8 (30.4–37.4) | <.001 | 37.4 (32.0–43.0) | 26.9 (19.1–36.3) | 0.05 |
eTable 2 shows the distribution of symptom characteristics, allergy severity and outcomes among adults with SA. Skin/mucosal and respiratory symptoms (e.g. nasal congestion and wheezing) were more commonly reported by crustacean compared to mollusk-allergic adults. In contrast, GI symptoms were more common among mollusk-allergic patients. Additionally, crustacean allergic adults may be more likely to develop shellfish allergy during adulthood (54.4%) compared to mollusk-allergic adults (45.8%) (p=0.11).
Table 2 reports adjusted associations among key demographic/comorbid atopic disease characteristics and SA outcomes. Adults reporting non-White races/ethnicity were more likely to have SA and crustacean allergy compared to their White (non-Hispanic) counterparts. Additionally, adults living in ocean-adjacent (shoreline) counties had elevated odds of having SA compared to those in non-shoreline counties (OR:1.2, 95% CI 1.1–1.4). Shoreline county residence was also significantly associated with having only crustacean allergy (i.e. no mollusk allergy), (OR: 1.3, 95% CI 1.1–1.6), however a similar trend was not observed with having only mollusk allergy.
Table 2.
Adjusted Associations for Demographics, Comorbid Diseases, and Severity of the Diagnosis Among Adults with Shellfish Allergy and Shellfish Allergy Subgroups.
| Variable | Odds of Convincing Shellfish Allergy Among All Adults (95% CI) | Odds of Convincing Crustacean Allergy Only Among All Adults (95% CI) | Odds of Convincing Mollusk Allergy Only Among All Adults (95% CI) | Odds of Severe Shellfish Reactions Among Adults with Convincing Shellfish Allergy (95% CI) | Odds of Severe Shellfish Reactions Among Adults with Convincing Crustacean Allergy Only (95% CI) | Odds of Severe Shellfish Reactions Among Adults with Convincing Mollusk Allergy Only (95% CI) | Adult Onset Shellfish Allergy Among Adults with Convincing Shellfish Allergy (95% CI) |
|---|---|---|---|---|---|---|---|
| Shoreline County | |||||||
| Yes vs. No | 1.2 (1. 1–1.4) | 1.3 (1.1–1.6) | 0.9 (0.6–1.4) | 0.8 (0.6–1.0) | 0.6 (0.4–0.9) | 0.8 (0.4–1.8) | 1.3 (1. 0–1.8) |
| Race/ethnicity (vs. White, non-Hispanic) | |||||||
| Asian, non-Hispanic | 1.7 (1.3–2.2) | 2.1 (1.5–3.0) | 1.7 (0.7–4.2) | 0.9 (0.5–1.7) | 1.1 (0.5–2.3) | 2.1 (0.5–9.5) | 1.0 (0.6–1.8) |
| Black, non-Hispanic | 1.3 (1.1–1.6) | 1.7 (1.3–2.2) | 0.8 (0.4–1.7) | 1.9 (1.2–2.8) | 2.2 (1.2–3.9) | 2.1 (0.6–7.1) | 1.0 (0.7–1.6) |
| Hispanic | 1.4 (1.1–1.7) | 1.3 (1.0–1.7) | 1.3 (0.7–2.4) | 1.2 (0.8–1.7) | 1.0 (0.6–1.7) | 1.2 (0.4–3.8) | 1.0 (0.7–1.5) |
| Multiple/other | 1.6 (1.1–2.3) | 1.7 (0.9–3.0) | 2.6 (1.3–5.2) | 0.6 (0.3–1.2) | 0.6 (0.2–2.0) | 1.6 (0.3–8.3) | 0.9 (0.5–1.6) |
| Sex | |||||||
| Female vs. Male | 1.5 (1.3–1.7) | 1.4 (1.1–1.8) | 1.4 (0.9–2.1) | 1.0 (0.7–1.3) | 1.0 (0.7–1.5) | 0.6 (0.3–1.3) | 1.6 (1.2–2.2) |
| Age (vs. <30 years) | |||||||
| 30–39 | 1.3 (1.1–1.6) | 1.4 (1.0–1.9) | 1.3 (0.7–2.4) | 0.8 (0.5–1.2) | 0.9 (0.5–1.7) | 0.4 (0.1–1.4) | 3.0 (1.9–4.9) |
| 40–49 | .9 (.7–1.1) | 1.0 (0.7–1.4) | 0.8 (0.4–1.4) | 1.1 (0.7–1.7) | 0.9 (0.5–1.8) | 1.2 (0.3–4.3) | 4.5 (2.7–7.4) |
| 50–59 | 1.2 (.9–1.5) | 1.3 (1.0–1.8) | 1.1 (0.6–1.9) | 0.9 (0.6–1.3) | 1.0 (0.5–1.8) | 0.5 (0.1–1.6) | 5.2 (3.2–8.4) |
| 60+ | .9 (.8–1.2) | 1.1 (0.8–1.5) | 0.9 (0.5–1.6) | 0.5 (0.3–0.7) | 0.5 (0.3–1.0) | 0.3 (0.1–0.9) | 14.4 (8.8–23.6) |
| Household income, $ | |||||||
| 25,000–49,999 | 1.0 (.8–1.2) | 1.0 (0.7–1.3) | 0.7 (0.4–1.3) | 0.8 (0.5–1.2) | 1.1 (0.6–2.0) | 0.3 (0.1–0.9) | 1.0 (0.7–1.6) |
| 50,000–99,999 | 1.2 (1.0–1.4) | 1.2 (.9–1.6) | 0.9 (0.5–1.6) | 0.8 (0.5–1.2) | 1.3 (0.7–2.2) | 0.3 (0.1–1.1) | 1.0 (0.7–1.5) |
| 100,000–149,000 | 1.1 (.9–1.4) | 1.2 (.9–1.7) | 1.0 (0.5–2.0) | 0.8 (0.5–1.3) | 1.5 (0.8–3.0) | 0.6 (0.1–2.5) | 1.2 (0.7–2.0) |
| >150,000 | .8 (.6–1.1) | .9 (.6–1.4) | 0.5 (0.2–1.1) | 0.8 (0.5–1.6) | 1.7 (0.7–4.1) | 0.9 (0.2–4.4) | 0.9 (0.5–1.7) |
| Comorbid Conditions (vs. not) | |||||||
| Asthma | 1.7 (1.4–2.0) | 1.9 (1.5–2.4) | 0.9 (0.5–1.4) | 1.1 (0.8–1.5) | 1.1 (0.7–1.7) | 1.1 (0.4–2.7) | 1.0 (0.7–1.4) |
| Atopic dermatitis | 1.4 (1.1–1.7) | 1.1 (.8–1.6) | 1.6 (0.5–1.4) | 1.6 (1.2–2.2) | 1.0 (0.5–2.0) | 0.5 (0.1–1.6) | 1.1 (0.7–1.8) |
| Allergic Rhinitis | 1.4 (1.2–1.7) | 1.3 (1.0–1.7) | 1.6 (1.1–2.4) | 1.6 (1.2–2.2) | 1.4 (0.9–2.3) | 2.5 (1.0–6.3) | 1.5 (1.0–2.0) |
| Insect Sting Allergy | 1.4 (1.1–1.8) | 1.2 (.8–1.8) | 1.4 (0.8–2.6) | 2.6 (1.5–4.5) | 2.7 (1.1–6.6) | 1.8 (0.5–6.9) | 0.8 (0.5–1.3) |
| Latex Allergy | 1.5 (1.1–2.0) | 1.3 (.8–2.1) | 0.8 (0.4–1.8) | 1.3 (0.6–2.5) | 1.5 (0.4–5.9) | 1.0 (0.3–3.8) | 0.8 (0.4–1.4) |
| Medication Allergy | 1.6 (1.4–2.0) | 1.9 (1.4–2.5) | 1.6 (1.1–2.4) | 0.9 (0.6–1.3) | 0.7 (0.4–1.3) | 1.4 (0.6–3.5) | 1.2 (0.8–1.9) |
| Urticaria/Hives | 1.6 (1.1–2.4) | 1.6 (.9–2.9) | 1.4 (0.5–3.8) | 0.8 (0.4–1.6) | 0.8 (0.3–2.3) | 0.7 (0.1–6.5) | 0.7 (0.3–1.7) |
Risk of severe shellfish reaction also differed by demographic characteristics, such that Black (non-Hispanic) race was associated with increased odds of severe reactions among adults with SA (OR:1.9, 95% CI, 1.2–2.8) and crustacean allergy (OR:2.2, 95% CI, 1.2–3.9), but not mollusk allergy (OR: 0.8 (0.4–1.7). Adults >60 years of age had decreased odds of having severe allergic reactions to shellfish (OR: 0.5, 95% CI 0.3–0.7), with a similar pattern reported for those with mollusk allergy (OR:0.3, 95% CI, 0.1–0.9). Interestingly, shoreline county residence appears to be linked to reduced odds of severe shellfish reactions (OR: 0.8, 95%CI (0.6–1.0) compared to those living in non-shoreline counties, with significant protective effects observed among adults with only crustacean allergy (OR:0.6, 95% CI 0.4–0.9). Data also indicate that current residence in a shoreline county may increase odds of adult-onset shellfish allergy (OR: 1.3, 95%CI 1.0–1.8). In addition, having a comorbid insect sting/venom allergy was associated with greater odds of having a severe crustacean allergy (OR: 2.7, 95%CI 1.1–6.6) while comorbid allergic rhinitis was associated with greater odds of a severe mollusk allergy (OR=2.5, 95%CI 1.0–6.3) as well as greater odds of adult-onset SA (OR:1.5, 95% CI 1.0–2.0).
Rates of comorbidities among shellfish and other food allergies are shown in eTable 3. The highest rates were observed among crustacean allergens and between crustacean and mollusk allergy. Fin fish allergy (18.4%) was the second most common allergy among adults with SA. Among adults with mollusk allergy, the most common accompanying allergy was shrimp (56.2%), followed by lobster (53.6%) and crab (53.1%) with an overall 70.2% cross-reactivity with crustacea.
Overall, SA is estimated to affect nearly 3% of US adults, half of whom report developing SA during adulthood. This updates national data collected in 2002, which reported adult SA prevalence rates of 2.6%, and also observed elevated rates among female and non-White adults8. In our study, adult mollusk allergy prevalence was 1.6%--significantly lower than the estimated crustacean allergy prevalence of 2.4%.
While nearly half (45%) of shellfish-allergic adults reported visiting the ED for food allergy treatment within their lifetime, not all adults with SA experience severe reactions. These data indicate that over 40% of shellfish-allergic adults report only mild-to-moderate reactions. Interestingly, reaction profiles appeared somewhat different among uniquely crustacean and mollusk-allergic adults, in that a greater proportion of adults with crustacean allergy reported skin/mucosal symptoms and wheezing symptoms with fewer gastrointestinal symptoms compared to mollusk-allergic adults. Crustacean-allergic adults also appear to have slightly higher rates of adult-onset SA compared to those with mollusk allergy.
Previous studies of coastal Asian populations reported high rates of SA, suggesting a relationship between greater shellfish allergen exposure and SA risk9. Here odds of current SA and crustacean allergy were significantly elevated among adults living in a shoreline county. However, despite presenting with an increased risk, crustacean-allergic adults residing in shoreline counties had decreased odds of severe reactions.
Despite previous research indicating high cross-reactivity among shellfish allergens4, limited epidemiological work has addressed this issue5. While Sicherer et al. (2004) reported that 14% of respondents with crustacean allergy also reported a mollusk allergy8, in our study 46% of crustacean-allergic adults were also mollusk-allergic. Strikingly, 70.2% of mollusk-allergic adults in our study were also crustacean-allergic, suggesting that there may be greater clinical cross-reactivity between crustacean and mollusk allergens than previously acknowledged. Moreover, nearly 1 in 5 adults with SA had comorbid fin fish allergy, with higher rates observed among mollusk-allergic adults. However, further studies incorporating standardized confirmatory allergy testing are clearly warranted to replicate these population-based, self-report survey data.
Given the substantial population-level burden of shellfish allergy identified here, we hope this study will raise awareness and spur further research to better understand, treat and prevent crustacean and mollusk allergies among US adults.
Supplementary Material
Acknowledgements:
The authors would like to thank the National Institute of Allergy and Infectious Disease for the financial support of the study (R21AI135702). Study PI and corresponding author Ruchi Gupta MD MPH had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Funding Source:
National Institute of Allergy and Infectious Disease; “US Prevalence, Distribution and Determinants of Adult and Childhood Food Allergy” (R21AI135702—PI: Gupta).
Footnotes
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Conflicts of Interest: Christopher Warren reports grant support from the National Institutes of Health. Dr. Aktas has no relationships to disclose. Dr. Gupta reports receiving grants from the National Institutes of Health (NIH), Stanford University, and Aimmune Therapeutics during the conduct of the study; serving as a medical consultant/advisor for DBV, Aimmune, Before Brands, Pfizer, Mylan, and Kaleo, Inc, over the past 3 years; and receiving grants from the NIH, Allergy and Asthma Network, Food Allergy Research & Education, Rho Inc, Northwestern University Clinical and Translational Sciences Institute, Thermo Fisher, United Health Group, Mylan, and the National Confectioners Association outside the submitted work. Dr. Davis reports research grants and contracts from the following entities: National Institute of Allergy and Infectious Disease, Aimmune Therapeutics, Inc. DBV Technologies Inc., ThermoFisher Scientific, Inc., Nutricia North America, Regeneron Pharmaceuticals, Moonlight Therapeutics, Inc.
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