Association of obesity with IgE levels and allergy symptoms in children and adolescents: Results from the National Health and Nutrition Examination Survey 2005-2006

Article Outline

• Abstract
• Methods
  • Study population
  • Allergy outcomes
  • Weight measurements
  • Other measures
  • Statistical analyses
• Results
• Discussion
• Fig E1. 
• Table E1. 
• Table E2. 
• Table E3. 
• References
• Copyright

Background

The prevalence of both obesity and allergic disease has increased among children over the last several decades. Previous literature on the relationship between obesity and allergic disease has been inconsistent. It is not known whether systemic inflammation could be a factor in this relationship.

Objective

We sought to examine the association of obesity with total and allergen-specific IgE levels and allergy symptoms in US children and adolescents and to assess the role of C-reactive protein.

Methods

National Health and Nutrition Examination Survey data from 2005-2006 included measurement of total and allergen-specific IgE levels and allergy questions. Overweight was defined as the 85th or greater to less than the 95th percentile of body mass index for age, and obesity was defined as the 95th percentile or greater. Linear and logistic regression models were used to examine the association of weight categories with total IgE levels, atopy, allergen-specific IgE levels, and allergy symptoms among youth aged 2 to 19 years.

Results

Geometric mean total IgE levels were higher among obese (geometric mean ratio, 1.31; 95% CI, 1.10-1.57) and overweight (ratio, 1.25; 95% CI, 1.02-1.54) children than among normal-weight children. The odds ratio (OR) for atopy (any positive specific IgE measurement) was increased in the obese children compared with that seen in those of normal weight; this association was driven largely by allergic sensitization to foods (OR for atopy, 1.26 [95% CI, 1.03-1.55]; OR for food sensitization, 1.59 [95% CI, 1.28-1.98]). C-reactive protein levels were associated with total IgE levels, atopy, and food sensitization.

Conclusions

Obesity might be a contributor to the increased prevalence of allergic disease in children, particularly food allergy. Systemic inflammation might play a role in the development of allergic disease.

Key words: Atopy, allergen-specific IgE, total IgE, body mass index, obesity, overweight, allergic disease, inflammation

Abbreviations used: BMI, Body mass index, CRP, C-reactive protein, DXA, Dual x-ray absorptiometry, NHANES, National Health and Nutrition Examination Survey, OR, Odds ratio

The adiposity of the US population has been growing steadily. This is true both for adults and children, and it is also the case throughout the developed countries of the world. This increase has been most apparent since about 1980. Before that time, only approximately 5% of US children aged 6 to 11 years were considered overweight; by 2004, that rate had climbed to nearly 19%.¹

Allergic disease has also been on the increase in recent decades. In the United States, from the period 1976-1980 to 1988-1994, the prevalence of skin test reactivity to 6 common allergens increased from 22% to 42%.² Increases in atopy have also been observed in Europe.³, ⁴, ⁵

Some researchers have shown obesity to be related to allergy symptoms or to higher serum IgE levels (a marker for atopy),⁶, ⁷, ⁸ whereas others have not.⁹, ¹⁰, ¹¹ Differences in the ages of the study populations, the specific outcomes examined, and the methods used for categorizing obesity might account for the disparate findings. Analyses of National Health and Nutrition Examination Survey (NHANES) III data collected in 1988-1994 showed neither the prevalence of atopy (defined by any positive skin test result) nor serum eosinophil counts (another marker for allergy) to be significantly related to increasing quartiles of body mass index (BMI) among children aged 6 to 17 years in adjusted models.¹² No IgE data were available in NHANES III.

Recent research suggests that systemic inflammation, as measured by using C-reactive protein (CRP) levels, might be important in the relationship between obesity and asthma.¹³ CRP is a marker for systemic inflammation, and its levels are often very high in overweight individuals. Differences in CRP levels by atopic status have not been previously examined. If CRP is associated with atopy as well, that would suggest a common pathway for the effect of being overweight on allergic disease and asthma.

An Allergy/Asthma Component was added to the 2005-2006 NHANES, which included total and allergen-specific serum IgE measurements. This is the largest nationally representative dataset of serum IgE levels that has ever been collected on the US population. This analysis explores the complex relationships between obesity, serum IgE levels, and allergy symptoms and examines how CRP plays a role in these relationships by using data from the 2005-2006 NHANES.

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Methods 

Study population 

The NHANES is a nationally representative survey conducted periodically to assess the health and nutritional status of adults and children in the United States. The primary purpose of NHANES is to determine the prevalence of major diseases and risk factors for those diseases.¹⁴ Details of the plan and operation of NHANES can be found online at http://www.cdc.gov/nchs/nhanes.htm. Written informed consent was obtained for all subjects.

The target population of NHANES is the civilian, noninstitutionalized population of the United States. The NHANES uses a stratified, multistage probability sampling design with oversampling of persons believed to be at increased health risk. The stages of sampling are (1) the primary sampling unit, which is usually a county or block of contiguous (low-population) counties; (2) segments within primary sampling units (blocks or clusters of households); (3) households within segments; and (4) 1 or more participants within households. Weights are supplied with the public use dataset so that estimates can be produced that reflect the US population distribution and can be considered to be nationally representative. Eligible persons 16 years or older are interviewed directly, whereas interviews for those younger than 16 years are done with a proxy. All persons who complete the household interview are invited to participate in the Medical Examination component of NHANES. In the 2005-2006 NHANES 4321 children aged 2 to 19 years completed both the interview and the medical examination components, and 4269 children had their heights and weights measured.

Allergy outcomes 

Allergy was determined in 2 ways: a questionnaire about symptoms and serum IgE measurement. The questionnaire that was added to NHANES in the 2005-2006 cycle asks individuals to report previous diagnoses of hay fever, eczema, and allergies. For those reporting a diagnosis, further questions are asked regarding age at diagnosis and occurrence of symptoms over the past year. This analysis uses current symptoms (ie, those occurring in the previous 12 months).

Participants aged 1 year and older were tested for total and allergen-specific serum IgE by using the Pharmacia Diagnostics ImmunoCAP 1000 System (Kalamazoo, Mich). A detailed description of the laboratory method can be found at the 2005-2006 NHANES Web page (http://www.cdc.gov/nchs/data/nhanes/nhanes_05_06/al_ige_d.pdf). Total IgE data are available for 3617 (84%) of the children aged 2 to 19 years. Because smaller quantities of serum were available for young children, the number and type of allergen-specific IgE tests performed varied by age. Children aged 1 to 5 years were tested for total IgE and specific IgE to dust mite (Dermatophagoides farinae and Dermatophagoides pteronyssinus), cat, dog, cockroach, Alternaria species, peanut, egg, and milk. Children and young adults aged 6 years and older also had specific IgE measurements for ragweed, ryegrass, Bermuda grass, white oak, birch, shrimp, Aspergillus species, thistle, mouse, and rat.

We defined atopy as a positive response (≥0.35 kU/L) to at least 1 of the allergens tested. Analysis of atopy included only individuals with information for the full panel of allergens (9 allergens for those <6 years of age and 19 for those 6-19 years of age). Of the 4321 children with a physical examination, 703 (16.3%) did not have enough blood for specific IgE testing, and 100 (2.3%) did not have a full panel. Except that younger children were more likely to be missing the blood sample, sociodemographic characteristics and prevalence of allergy (by questionnaire) did not differ between those with IgE measurements and those without.

Weight measurements 

All participants who attended the medical examination had their weights and heights measured according to a standard protocol. BMI was calculated as weight in kilograms divided by height in meters squared. The sex-specific BMI percentile for age was calculated by using the US Centers for Disease Control and Prevention 2000 reference standards.¹⁵ Children between the 5th and 85th percentiles of BMI for age were considered to be normal weight, those between the 85th and 95th percentiles were considered overweight, and those at or above the 95th percentile were considered obese, as recommended by the American Medical Association.¹⁶

Other measures 

The age, sex, and race/ethnicity of the child, as reported in the personal interview, were examined as potential confounders and effect modifiers. As measures of socioeconomic status, the highest education level obtained by the household reference person (typically the household head) and quartiles of the poverty income ratio were also examined for their relationship to overweight status and atopy. The poverty income ratio is the relationship of family income to the poverty threshold based on family size and composition.¹⁷

Other potential confounders considered were current household smoking (yes/no), maternal smoking during pregnancy (yes/no), birth weight (low birth weight vs not), and several physical activity measures. All children were asked the average number of hours per day they spent either watching television or using a computer. For children age 2 to 11 years, the proxy respondent answered 1 question about how many times per week the child played or exercised enough to sweat or breathe hard. Children aged 12 to 19 years answered more detailed questions about the specific activities that qualified as moderate or vigorous activity and the number of times they performed those activities in the past month. For this analysis, the number of times vigorous activities were reported were summed and recalculated as a weekly rather than a monthly total to make this information comparable with that for the younger children.

Statistical analyses 

Because underweight status has been associated with increased risk for allergic disease,¹⁸ we excluded 144 children who were less than the 5th percentile of BMI for their age and sex (3.4%). Of the 4125 children and adolescents above this cutoff point, 4111 have data on allergy symptoms, and 3387 have data for atopy.

The association of overweight status with geometric mean total IgE levels was estimated by using the ratio of the geometric means in a linear regression model. Logistic regression was used to determine the prevalence odds ratio (OR) for weight category in relation to atopy, a positive test result to any food allergen, a positive test result to any inhalant allergen (the nonfood allergens), a positive test result to any perennial allergen (dust mite, cockroach, mold, cat, dog, rat, and mouse), a positive test result to any seasonal allergen (trees and grasses), and a positive response to the following allergic symptom outcomes: the occurrence of allergy symptoms or attacks in the past year (yes/no), the occurrence of hay fever symptoms in the past year (yes/no), and eczema (itchy rash coming and going for ≥6 months in the past year, yes/no). In addition, weight was examined in relation to each allergen individually.

The association between continuous BMI percentile for age and total IgE levels (logbase 10) was examined by using linear regression. Data were plotted by using a scatterplot smoothing technique.¹⁹

Potential modification of the effect of overweight status on atopy and allergic outcomes was examined for sex, age, and race/ethnicity. A P value for the interaction term of less than .10 was considered evidence of interaction. Stratified models were used to explore associations where evidence for interaction was found.

The potential for confounding was first examined by looking at the strength of the univariate associations between potential available confounders and the exposure and outcome. Age, sex, race/ethnicity, poverty income ratio, and household smoking were retained in the adjusted models based on these associations and findings from previous studies. Results for both simple age-adjusted and fully adjusted models are shown. CRP was found to be associated with both weight and atopy but cannot be treated as a confounder in this relationship because it might be on the causal pathway. Instead, a model that assessed the relationship between CRP levels and atopy and potential confounding by BMI examined this possibility.

All analyses were performed with the SAS survey sampling procedures to adjust for the NHANES complex sampling design (version 9.1.3; SAS Institute, Inc, Cary, NC). Figures were generated by using the R system for statistical computing (version 2.7.0), which also can account for the sampling design.¹⁹

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Results 

Table I shows the distribution of the allergic outcomes in the NHANES 2005-2006 population aged 2 to 19 years by demographic characteristics and other potential confounding variables. Total IgE levels increased with age and were higher among boys. By race/ethnicity, IgE levels were highest in non-Hispanic blacks and lowest in non-Hispanic whites. Total IgE levels were higher with a lower poverty income ratio. There is also a strong relationship between CRP levels and total IgE levels. Total IgE levels were not related to smoking, birth weight, or physical activity.

Table I. Distribution of total serum IgE levels, atopy, and recent allergy symptoms by population characteristics, NHANES 2005-2006, children aged 2 to 19 years

Subject characteristics	N	Percent incategory	Geometric mean total IgE (SE)	P value∗	Percentage (SE) atopic†	OR (95% CI)	Percentage (SE) withallergy symptoms	OR (95% CI)
Overall	4111		50.4 (2.5)		46.4 (0.9)		18.7 (1.4)
Age (y)
2-5	918	21.0	35.2 (3.9)	<.0001	37.5 (2.1)	1.00	14.8 (2.1)	1.00
6-10	904	28.4	52.9 (3.7)		46.3 (2.5)	1.44 (1.02-2.02)	20.8 (2.3)	1.51 (1.01-2.23)
11-14	929	21.6	50.6 (4.0)		45.2 (2.1)	1.38 (1.07-1.77)	17.4 (1.9)	1.21 (0.81-1.81)
15-19	1360	29.0	59.2 (6.3)		52.1 (2.4)	1.82 (1.32-2.49)	20.6 (2.2)	1.49 (1.09-2.04)
Sex
Male	2031	51.0	60.8 (3.7)	.0002	49.4 (1.7)	1.29 (1.09-1.52)	19.1 (1.9)	1.05 (0.82-1.35)
Female	2080	49.0	41.4 (2.7)		43.2 (1.1)	1.00	18.4 (1.6)	1.00
Race/ethnicity
Non-Hispanic white	1074	59.6	41.4 (3.0)	<.0001	42.2 (1.5)	1.00	21.8 (2.4)	1.00
Non-Hispanic black	1291	14.9	83.9 (5.9)		62.2 (1.8)	2.26 (1.82-2.79)	17.5 (1.7)	0.76 (0.50-1.16)
Mexican American	1371	13.3	55.6 (3.2)		47.4 (1.7)	1.23 (1.01-1.51)	10.7 (0.9)	0.43 (0.30-0.63)
Other	375	12.2	66.6 (8.7)		47.6 (3.7)	1.24 (0.90-1.72)	14.0 (2.4)	0.58 (0.34-0.98)
Education (family referent)
<12th grade	1280	18.9	62.6 (4.9)	.02	46.7 (2.2)	0.99 (0.84-1.17)	9.3 (1.4)	0.38 (0.23-0.62)
12th grade/GED	930	24.7	45.4 (4.6)		46.2 (1.6)	0.97 (0.77-1.22)	19.5 (1.8)	0.88 (0.63-1.24)
>12th grade	1722	52.9	49.0 (3.4)		46.9 (1.7)	1.00	21.5 (2.2)	1.00
Poverty income ratio (quartiles)
1st	1474	24.2	62.9 (3.1)	.003	49.0 (1.8)	1.11 (0.88-1.39)	13.7 (1.2)	0.52 (0.39-0.69)
2nd	1064	24.2	51.3 (6.0)		44.9 (2.2)	0.94 (0.68-1.29)	19.1 (2.2)	0.77 (0.53-1.12)
3rd	755	24.2	45.4 (3.2)		45.5 (2.1)	0.96 (0.78-1.19)	18.5 (2.5)	0.74 (0.52-1.07)
4th	617	24.1	43.5 (3.2)		46.5 (2.6)	1.00	23.4 (3.0)	1.00
Missing/unknown	201	3.3	54.0 (9.5)		43.2 (6.0)		19.8 (3.4)
Any smokers in household
Yes	667	16.3	53.5 (5.6)	.61	44.3 (3.1)	0.90 (0.64-1.25)	20.4 (1.7)	1.13 (0.91-1.40)
No	3398	83.7	49.9 (3.0)		47.0 (1.4)	1.00	18.5 (1.5)	1.00
Mother smoked during pregnancy‡
Yes	436	18.0	50.1 (2.6)	.74	39.2 (2.7)	0.75 (0.59-0.96)	21.1 (1.9)	1.27 (1.00-1.62)
No	2555	82.0	47.9 (2.6)		46.1 (1.1)	1.00	17.3 (1.6)	1.00
Birth weight‡
<2500 g	278	8.0	49.0 (6.3)	.87	41.4 (3.9)	0.86 (0.60-1.24)	12.9 (2.6)	0.65 (0.37-1.13)
≥2500 g	2692	92.0	48.0 (2.5)		45.2 (1.2)	1.00	18.6 (1.7)	1.00
Physical activity
0-3 times/wk	1454	32.9	48.2 (4.4)	.33	45.9 (1.7)	0.85 (0.65-1.10)	19.5 (1.7)	1.08 (0.83-1.40)
4-6 times/wk	730	19.0	49.8 (5.1)		48.2 (2.4)	0.93 (0.71-1.21)	19.7 (2.0)	1.09 (0.89-1.34)
7 times/wk	1100	17.9	49.7 (4.9)		43.6 (2.1)	0.77 (0.61-0.97)	17.9 (2.4)	0.98 (0.66-1.43)
≥8 times/wk	752	18.3	57.1 (5.8)		50.1 (2.4)	1.00	18.3 (2.1)	1.00
Average hours of TV/videos
0 h/d	531	15.5	49.6 (5.1)	.29	49.9 (2.5)	1.00	19.0 (2.5)	1.00
1-2 h/d	2002	54.9	47.0 (2.7)		45.2 (1.4)	0.83 (0.66-1.04)	18.4 (2.1)	0.96 (0.66-1.40)
≥3 h/d	1508	29.7	58.2 (5.2)		46.9 (2.5)	0.89 (0.67-1.16)	19.8 (1.8)	1.05 (0.80-1.39)
Average hours of computer use
0 h/d	1300	36.6	50.1 (2.8)	.89	46.0 (1.8)	1.00	20.0 (2.0)	1.00
1-2 h/d	1155	29.9	52.2 (4.0)		46.8 (1.7)	1.03 (0.82-1.29)	20.2 (2.3)	1.01 (0.72-1.42)
≥3 h/d	1581	33.5	49.6 (3.9)		46.6 (1.5)	1.02 (0.90-1.17)	16.4 (2.0)	0.78 (0.53-1.16)
CRP§
Not detectable	860	23.9	42.2 (2.6)	.0008	42.8 (1.9)	1.00	17.1 (2.3)	1.00
0.2–0.4 mg/L	834	20.8	49.2 (4.7)		42.5 (2.7)	0.99 (0.79-1.24)	18.1 (2.9)	1.07 (0.67-1.69)
0.4–1.4 mg/L	804	18.7	55.0 (3.2)		51.7 (2.6)	1.43 (1.07-1.92)	18.5 (2.1)	1.10 (0.73-1.65)
>1.4–13.6 mg/L	888	19.1	62.5 (5.9)		50.8 (2.4)	1.38 (1.11-1.72)	20.7 (2.3)	1.26 (0.93-1.72)
Missing/unknown	725	17.6	30.6 (8.0)		35.6 (6.0)		19.8 (2.1)

The proportion classified as atopic based on at least 1 positive allergen-specific IgE result follows a similar pattern, with boys being more likely than girls to be atopic, and non-Hispanic blacks and Mexican Americans being more likely than non-Hispanic whites to be atopic. Children whose mothers smoked during pregnancy were somewhat less likely to be atopic than children of nonsmoking mothers. Atopy was also related to the child's CRP level.

Odds of current allergy symptoms were increased at older ages but reduced for Mexican Americans. Children whose household reference person had less than a high school education and those in the lowest quartile of poverty income ratio also had a reduced odds of recent allergy symptoms. Otherwise, a report of recent allergy symptoms was not highly associated with any of the sociodemographic characteristics.

The relationships of the same characteristics to obesity are shown in Table E1 (available in this article's Online Repository at www.jacionline.org). Overweight status was associated with older age, being non-Hispanic black or Hispanic, lower education, smoking, and lower physical activity levels, especially the number of hours of television watching. As expected, there is a moderate relationship of obesity with CRP levels. The correlation between the continuous BMI z score and the log10 CRP level is 0.39 (95% CI, 0.37-0.41).

Table II shows the age-adjusted and fully adjusted association of the overweight categories with total IgE levels, atopy, sensitization to food and inhalant allergens, and reported allergy symptoms, hay fever, and eczema. Both weight categories were associated with higher total IgE levels in both models. Being in the obese category was associated with higher odds of atopy (OR, 1.26; 95% CI, 1.03-1.55). The OR for sensitization to foods was particularly increased (OR, 1.59; 95% CI, 1.28-1.98), whereas the odds for inhalant allergen sensitization were not increased in the fully adjusted model. Odds for allergy symptoms, hay fever, and itchy rash were also not different by weight category in adjusted models. Examination of the specific foods tested shows a large association with sensitization to milk in both weight categories, an association with sensitization to egg in the overweight category only, and an association with sensitization to shrimp in the obese category only. There was no association observed for sensitization to peanut. With the exception of total IgE levels, significant sex differences were not observed; however, data are presented by sex in Table E2 (available in this article's Online Repository at www.jacionline.org). Although no significant effect modification was seen by age group for these outcomes (see Table E3 available in this article's Online Repository at www.jacionline.org), the food sensitization association in the 2- to 5-year-old children was particularly strong (OR, 2.58; 95% CI, 1.45-4.60).

Table II. Allergic outcomes by weight category (BMI percentile for age), NHANES 2005-2006, children and young adults aged 2 to 19 years

Allergy outcome	Measure (SE)	Ratio∗ (95% CI), age-adjusted model†	Ratio∗ (95% CI), fully adjustedmodel‡
Total IgE, geometric mean (kU/L)
Normal weight	45.7 (2.6)	1.00	1.00
Overweight	57.8 (5.1)	1.22 (0.99-1.51)	1.25 (1.02-1.54)
Obese	66.6 (5.8)	1.40 (1.19-1.66)	1.31 (1.10-1.57)
Any positive specific IgE measurement (%)
Normal weight	44.5 (1.3)	1.00	1.00
Overweight	48.9 (2.6)	1.14 (0.91-1.44)	1.16 (0.93-1.45)
Obese	51.8 (2.1)	1.28 (1.05-1.58)	1.26 (1.03-1.55)
Any positive food IgE measurement (%)
Normal weight	21.1 (0.9)	1.00	1.00
Overweight	24.4 (2.0)	1.26 (0.99-1.60)	1.27 (0.98-1.65)
Obese	29.2 (2.2)	1.61 (1.30-1.98)	1.59 (1.28-1.98)
Positive egg IgE measurement (%)
Normal weight	5.2 (0.6)	1.00	1.00
Overweight	8.8 (1.5)	2.22 (1.36-3.62)	2.26 (1.35-3.80)
Obese	4.7 (1.1)	1.12 (0.71-1.77)	1.19 (0.74-1.92)
Positive milk IgE measurement (%)
Normal weight	10.0 (0.9)	1.00	1.00
Overweight	12.5 (2.0)	1.62 (1.22-2.13)	1.54 (1.10-2.15)
Obese	12.1 (1.4)	1.56 (1.20-2.03)	1.52 (1.18-1.98)
Positive peanut IgE measurement (%)
Normal weight	9.7 (1.1)	1.00	1.00
Overweight	8.4 (1.5)	0.81 (0.52-1.26)	0.83 (0.52-1.33)
Obese	11.8 (1.7)	1.18 (0.78-1.79)	1.12 (0.74-1.72)
Positive shrimp IgE measurement (%)
Normal weight	5.2 (0.5)	1.00	1.00
Overweight	5.3 (1.7)	0.97 (0.52-1.81)	0.94 (0.49-1.78)
Obese	10.6 (1.3)	2.08 (1.62-2.66)	1.88 (1.36-2.60)
Any positive inhalant IgE measurement (%)
Normal weight	39.2 (1.4)	1.00	1.00
Overweight	42.7 (3.2)	1.05 (0.80-1.37)	1.08 (0.83-1.42)
Obese	45.6 (2.7)	1.18 (0.95-1.48)	1.17 (0.91-1.50)
Allergy symptoms in previous year (%)
Normal weight	19.3 (1.5)	1.00	1.00
Overweight	18.1 (2.0)	0.90 (0.73-1.10)	0.96 (0.77-1.20)
Obese	17.0 (1.7)	0.83 (0.68-1.02)	0.90 (0.74-1.10)
Hay fever in previous year (%)
Normal weight	2.9 (0.7)	1.00	1.00
Overweight	2.0 (0.9)	0.66 (0.24-1.81)	0.68 (0.23-1.99)
Obese	3.5 (0.8)	1.19 (0.61-2.32)	1.37 (0.71-2.62)
Itchy rash in previous year (%)
Normal weight	6.0 (0.7)	1.00	1.00
Overweight	8.3 (1.7)	1.50 (0.79-2.85)	1.58 (0.82-3.05)
Obese	7.9 (1.7)	1.43 (0.96-2.13)	1.50 (0.96-2.32)

Fig 1 shows the relationship between continuous BMI percentile for age and total IgE levels stratified by sex. There is a significant linear trend (for a 1-SD increase in the BMI z score on the log10 value of total IgE) that is stronger for girls (slope, 0.104; 95% CI, 0.064-0.143) than for boys (slope, 0.042; 95% CI, 0.010-0.075; P for interaction = .04). Race/ethnicity modified the relationship between overweight status and atopy in girls (see Table E3). Fig 2 displays the percentage of atopy among girls by ethnicity and weight category. The association of obesity with atopy was only significant among non-Hispanic white and non-Hispanic black girls.

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• Fig 1. 

  Association between BMI percentile for age and total IgE level by sex, NHANES 2005-2006, children age 2 to 19 years. The shaded region represents the 95% confidence limits of the data. The black lines represent observations and show where the data lie on the BMI distribution. The x-axis is plotted as the z score for BMI for age and labeled with the transformation of z scores to percentiles.

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• Fig 2. 

  Prevalence of atopy by race and weight status among girls, NHANES 2005-2006, children age 2 to 19 years. The dots reflect the mean prevalence of atopy, and the bars represent the 95% CI.

To examine whether CRP levels (ie, systemic inflammation) might be on the pathway between obesity and atopy, we examined whether CRP levels were related to total IgE levels, atopy, and food allergy with and without adjustment for BMI (Table III). CRP and total IgE levels were correlated in age-adjusted analysis. Further adjustment for race, socioeconomic status, and smoking attenuated the relationship. Adjusting for BMI in addition to sociodemographic factors decreased the model estimate by 31% (12% in boys and 70% in girls). Thus the relationship of CRP levels to total IgE levels was confounded by BMI. Conversely, the OR for atopy was not significantly attenuated when adjusting for BMI, and the OR for food sensitization was reduced by more than 10% only in girls.

Table III. Effect estimate for a log10 increase in CRP levels before and after adjustment for poverty, race, household smoking, and BMI z score, NHANES 2005-2006, children aged 2 to 19 years

	Age-adjusted		+ Poverty, race, smoking		+ BMI z score
	Estimate	95% CI	Estimate	95% CI	Estimate	95% CI	Change∗
Total IgE level
Overall	0.087	0.036 to 0.137	0.084	0.032 to 0.136	0.058	−0.009 to 0.124	31%
Boys	0.090	0.007 to 0.172	0.095	0.007 to 0.183	0.084	−0.010 to 0.177	12%
Girls	0.091	0.032 to 0.149	0.066	−0.001 to 0.133	0.020	−0.070 to 0.110	70%
Atopy
Overall	1.22	1.07 to 1.41	1.26	1.07 to 1.49	1.22	1.00 to 1.49	3%
Boys	1.28	1.10 to 1.47	1.37	1.15 to 1.64	1.36	1.09 to 1.70	1%
Girls	1.20	1.02 to 1.42	1.15	0.96 to 1.37	1.07	0.89 to 1.30	7%
Food allergy
Overall	1.31	1.11 to 1.55	1.36	1.13 to 1.64	1.25	1.01 to 1.55	8%
Boys	1.26	0.98 to 1.61	1.34	1.01 to 1.77	1.26	0.90 to 1.76	6%
Girls	1.41	1.16 to 1.71	1.39	1.10 to 1.74	1.21	0.97 to 1.52	14%

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Discussion 

We found a relationship between overweight status and atopy in this population of American children aged 2 to 19 years. Sensitization to foods appeared to be responsible for the overall relationship with atopy. For most of the outcomes, the associations were stronger for the obese weight category than the overweight category, providing evidence of a dose response for weight. The analysis of continuous BMI with total IgE levels supports the concept that increased weight is associated with increased allergic predisposition.

A relationship between obesity and atopy has been observed before, although not consistently, and food sensitization has rarely been examined in relation to body weight. Huang et al⁶ found that Taiwanese teenage girls in the highest quintile of BMI were more likely to be atopic than girls in the middle 3 quintiles (OR, 1.77; 95% CI, 1.15-2.73). Xu et al⁸ found atopy to be associated with current BMI among Finnish adults. Schachter et al⁷ combined data from 7 epidemiologic studies in Australian children and found that BMI was associated with atopic status among girls only. In all of these studies, skin prick test responses were used rather than allergen-specific serum IgE levels, and only the Huang et al⁶ study included a food allergen (shellfish mix) among the allergens tested. In contrast, the European Community Respiratory Health Survey used allergen-specific IgE levels (dust mite, grass, or cat) to define atopy and did not find a relationship with BMI among young adults.⁹

Previous work with NHANES III data also did not find a significant relationship between overweight status and atopy in children age 6 to 17 years.¹² Comparative analyses with both datasets suggest that the main reasons for this difference are the inclusion of younger children and the inclusion of the food-specific IgE tests in 2005-2006 NHANES. Although a significant interaction effect was not seen overall across age groups, the largest OR was observed among the 2- to 5-year-old children (OR, 2.58; 95% CI, 1.45-4.60). Additionally, our findings were strongest for food-specific IgE levels. The 2005-2006 NHANES data include IgE levels for milk, egg, peanut, and shrimp, whereas NHANES III data included only a skin test for peanut. Sensitizations to milk (more common in younger children) and to shrimp (only tested in those ≥6 years) were both strongly associated with overweight status and obesity. The association with sensitization to shrimp suggests that the relationship is not limited to egg and milk allergy or to younger children.

Conversely, no association was seen between obesity and reported allergy symptoms and hay fever. The symptom outcomes and IgE levels are weakly correlated in these data. This could be in part because the symptom data relate to only the 12 months before the survey, whereas serum IgE levels reflect overall allergic predisposition. In addition, the persons with the most allergy symptoms might take regular medication and thus might not report having an allergy attack. Information on over-the-counter allergy medication, however, is not available in the NHANES 2005-2006 dataset.

Effect modification by sex was observed for total IgE levels but not the other allergic outcomes. Total IgE levels were increased for girls (but not boys) in the overweight category, whereas they were increased for boys (but not girls) in the obese category. In addition, the relationship of BMI examined as a continuous variable with total IgE levels was stronger in girls than in boys. In girls the effect on atopy was present among non-Hispanic white and black girls but not Mexican American girls. The mechanism for this difference among racial/ethnic groups remains enigmatic, especially given that obesity and atopy were strongly associated among Mexican American boys.

One limitation of this analysis is that it used BMI to characterize obesity, which is not a direct measure of fatness and might misclassify some children, particularly adolescent males, who can be heavier than average because of a larger bone structure or more muscle mass.²⁰ Nevertheless, BMI has been shown to correlate well with other measures of adiposity. Mei et al²¹ compared BMI with dual x-ray absorptiometry (DXA) in a pooled dataset of 3 studies in children and found correlations that ranged from 0.78 to 0.88 and that the area under the receiving operating characteristics curve was 0.952. DXA to directly measure the percentage of body fat was performed in the 2005-2006 NHANES, but those data are not available at this time. To assess the potential for bias, we examined the correlation between percentage body fat, as measured by means of DXA, and BMI in the available NHANES data from 1999-2004 (See Fig E1 in the Online Repository at www.jacionline.org). We found the correlation between BMI z scores and percentage body fat to be 0.78 overall. The correlation was somewhat weaker (0.73) for adolescent boys but otherwise did not differ significantly by sex, race, or age. BMI was observed to perform poorly as a proxy for percentage body fat only among children below the 50th percentile, suggesting that the potential for misclassification of weight status when using the US Center for Disease Control and Prevention's BMI percentile for age categories at the upper end of the distribution is minimal.

ORs, as presented in this study, always overestimate the true relative risk but are a reasonably good estimate for rare outcomes.²² Because the prevalence of atopy is high in US children (46%), the estimated OR is considerably farther from the null than the relative risk. Nonetheless, reported P values and CIs remain valid.

The relationship between CRP levels and atopy has not been previously examined. Because we found a relationship between CRP levels and atopy in this study, we explored the possibility that inflammation (CRP) could be on the pathway between obesity and atopy. Because it is inappropriate to control for such an intermediate variable as a confounder,²² we tested whether the intermediate (CRP) was related to total IgE levels, atopy, and food sensitization and whether that relationship was confounded by BMI. We found that CRP levels were positively correlated to total IgE levels and that confounding of this relationship by BMI was indeed present. This suggests that there could be an inflammatory component to the association between BMI and IgE levels. We were not able, however, to demonstrate the same level of confounding for atopy or food sensitization, except for girls in the latter case.

Importantly, because these NHANES data come from a cross-sectional survey, it is not possible to assign causality to these associations. Other explanations for our findings are possible, such as the presence of an unmeasured confounder, like gut microbiota,²³ which is known to be associated with both increased allergy and obesity. Given that some sex differences were observed, hormonal influences might also be at play. Reverse causation could also be possible if children with milk allergy drink more juice or sweetened beverages, which have been shown to increase obesity in children.²⁴, ²⁵ It will be necessary to examine interrelationships among overweight status, systemic inflammation, and atopy in a prospective fashion to understand the true causal mechanisms that underlie the relationships between adiposity and the development and manifestation of atopy and allergic symptoms.

NHANES 2005-2006 is the largest dataset of serum IgE levels that has ever been collected, and it comes from a sample that is generalizable to the population of the United States. NHANES uses standardized data collection methods with strict quality control and contains a wealth of data regarding every study subject. Our analysis, using an objective assessment of atopy, shows that overweight status in children is associated with allergic predisposition, especially to food. Childhood obesity might be the most important health issue facing US children today. Although an increase in allergy might not be the most consequential health risk faced by overweight children, it does provide additional motivation for undertaking the difficult challenge to reduce childhood obesity.

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Fig E1. 

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• Correlation between percentage body fat measured by means of DXA and BMI z score by age group (in quintiles), sex, and race/ethnicity in unweighted data from NHANES 1999-2004. The dark gray line represents the median BMI, and the light gray lines represent the 85th and 95th percentiles of BMI for age and sex. The correlation (with 95% CI) is given overall and above and below the median value for each age/sex group.

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Table E1. 

Distribution of overweight by population characteristics, NHANES 2005-2006, children and young adults aged 2 to 19 years

Subject characteristics	N	Percentage (SE) overweight	OR (95% CI)	Percentage (SE) obese	OR (95% CI)
Overall	4111	14.2 (0.9)		16.6 (1.3)
Age (y)
2-5	918	10.7 (1.7)	1.00	11.0 (1.5)	1.00
6-10	904	12.9 (2.1)	1.32 (0.79-2.21)18)	15.7 (2.1)	1.56 (0.96-2.55)
11-14	929	16.0 (2.2)	1.86 (1.24-2.78)18)	21.3 (3.4)	2.40 (1.51-3.83)
15-19	1360	16.6 (1.4)	1.85 (1.32-2.59)	18.0 (2.0)	1.95 (1.30-2.92)
Sex
Male	2031	14.2 (1.2)	1.02 (0.87-1.21)	17.2 (1.4)	1.10 (0.94-1.30)
Female	2080	14.1 (0.9)	1.00	15.9 (1.4)	1.00
Race/ethnicity
Non-Hispanic white	1074	14.3 (1.3)	1.00	14.1 (1.7)	1.00
Non-Hispanic black	1291	14.2 (1.1)	1.12 (0.85-1.48)	21.9 (1.6)	1.74 (1.24-2.46)
Mexican American	1371	16.1 (0.8)	1.34 (1.06-1.70)	23.7 (1.8)	2.00 (1.48-2.72)
Other	375	11.4 (1.9)	0.78 (0.52-1.16)	14.4 (2.3)	0.99 (0.62-1.58)
Education (family referent)
<12th grade	1280	15.3 (1.9)	1.28 (0.94-1.76)	19.5 (1.4)	1.50 (1.22-1.85)
12th grade/GED	930	14.9 (1.7)	1.24 (0.86-1.79)	19.2 (1.9)	1.46 (1.15-1.86)
>12th grade	1722	13.2 (1.1)	1.00	14.4 (1.5)	1.00
Poverty index (quartiles)
1st	1474	15.0 (1.6)	1.30 (0.87-1.95)	20.4 (1.8)	1.80 (1.31-2.47)
2nd	1064	13.5 (1.2)	1.11 (0.85-1.46)	18.3 (1.5)	1.53 (0.94-2.50)
3rd	755	14.9 (2.5)	1.18 (0.75-1.86)	14.2 (2.5)	1.15 (0.69-1.90)
4th	617	13.1 (1.3)	1.00	13.0 (2.2)	1.00
Missing/unknown	201	16.0 (2.4)		20.0 (4.2)
Any smokers in household
Yes	667	15.2 (2.2)	1.17 (0.88-1.56)	20.0 (2.4)	1.36 (0.97-1.89)
No	3398	14.0 (0.9)	1.00	15.9 (1.4)	1.00
Mother smoked during pregnancy
Yes	436	13.3 (1.2)	1.04 (0.78-1.39)	19.6 (2.4)	1.39 (1.00-1.92)
No	2555	13.6 (1.1)	1.00	15.0 (1.5)	1.00
Birth weight
<2500 g	278	12.0 (3.8)	0.82 (0.43-1.56)	13.0 (3.3)	0.75 (0.45-1.24)
≥2500 g	2692	13.6 (0.8)	1.00	16.1 (1.4)	1.00
Physical activity
0-3 times/wk	1454	13.7 (1.3)	0.81 (0.62-1.04)	21.3 (1.6)	1.57 (1.12-2.20)
4-6 times/wk	730	14.3 (1.4)	0.78 (0.50-1.21)	15.0 (2.2)	1.02 (0.75-1.38)
7 times/wk	1100	12.3 (2.1)	0.64 (0.37-1.11)	14.1 (1.4)	0.92 (0.56-1.51)
≥8 times/wk	752	17.8 (2.4)	1.00	14.2 (2.7)	1.00
Average hours of TV/videos
0 h/d	531	12.4 (2.5)	1.00	8.6 (1.4)	1.00
1-2 h/d	2002	14.2 (1.1)	1.28 (0.79-2.09)	15.6 (1.4)	2.03 (1.37-3.02)
≥3 h/d	1508	14.9 (1.2)	1.52 (0.94-2.45)	22.8 (2.5)	3.35 (2.09-5.37)
Average hours of computer
0 h/d	1300	13.3 (1.4)	1.00	16.1 (1.8)	1.00
1-2 h/d	1155	16.3 (1.7)	1.32 (0.92-1.90)	18.1 (1.9)	1.21 (0.90-1.62)
≥3 h/d	1581	13.1 (1.4)	0.98 (0.70-1.35)	15.8 (1.3)	0.98 (0.78-1.26)
CRP protein∗
Not detectable	860	7.9 (0.9)	1.00	1.8 (0.5)	1.00
0.02–0.04 g/dL	834	14.2 (1.3)	2.19 (1.60-3.00)	11.9 (1.9)	8.14 (5.36-12.4)
0.04–0.14 mg/dL	804	19.3 (1.7)	3.82 (2.94-4.97)	23.1 (2.1)	20.2 (10.8-37.9)
>0.14 mg/dL	888	18.4 (2.6)	4.66 (3.23-6.73)	36.5 (3.4)	40.9 (26.4-63.3)
Missing/unknown	725	12.5 (1.7)		13.8 (2.2)

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Table E2. 

Allergic outcomes by weight category (BMI percentile for age), NHANES 2005-2006, children and young adults aged 2 to 19 years

	Boys (n = 2031)			Girls (n = 2080)
Allergy outcome	Measure (SE)	Ratio∗ (95% CI), unadjusted model†	Ratio∗ (95% CI), adjusted model†	Measure (SE)	Ratio∗ (95% CI), unadjusted model†	Ratio∗ (95% CI), adjusted model†	Interaction P value
Total IgE, geometric mean (kU/L)
Normal weight	56.4 (4.2)	1.00	1.00	36.6 (2.3)	1.00	1.00	.02
Overweight	57.7 (4.6)	1.02 (0.80-1.29)	1.02 (0.78-1.34)	58.0 (7.8)	1.45 (1.12-1.87)	1.47 (1.16-1.86)
Obese	84.3 (10.9)	1.47 (1.16-1.86)	1.42 (1.12-1.80)	50.8 (6.9)	1.30 (1.00-1.70)	1.19 (0.89-1.57)
Any positive specific IgE result (%)
Normal weight	48.3 (2.2)	1.00	1.00	40.5 (1.2)	1.00	1.00	.54
Overweight	50.8 (3.5)	1.08 (0.78-1.48)	1.10 (0.80-1.52)	47.0 (3.5)	1.25 (0.90-1.72)	1.21 (0.86-1.71)
Obese	52.5 (4.1)	1.12 (0.78-1.61)	1.20 (0.89-1.63)	50.9 (2.3)	1.48 (1.22-1.79)	1.32 (1.06-1.64)
Any positive food IgE result (%)
Normal weight	24.3 (1.8)	1.00	1.00	17.8 (0.8)	1.00	1.00	.62
Overweight	26.1 (3.4)	1.12 (0.79-1.60)	1.13 (0.80-1.62)	22.7 (2.8)	1.45 (1.01-2.08)	1.44 (0.97-2.12)
Obese	31.7 (3.6)	1.50 (1.12-2.03)	1.60 (1.16-2.23)	26.2 (2.2)	1.73 (1.38-2.16)	1.56 (1.20-2.03)
Any positive inhalant IgE result (%)
Normal weight	43.0 (2.5)	1.00	1.00	35.1 (1.3)	1.00	1.00	.45
Overweight	44.3 (4.8)	1.00 (0.64-1.56)	1.01 (0.65-1.57)	41.1 (3.3)	1.14 (0.85-1.51)	1.14 (0.83-1.56)
Obese	45.5 (4.6)	0.99 (0.67-1.48)	1.04 (0.72-1.52)	45.7 (2.5)	1.43 (1.18-1.74)	1.29 (1.01-1.63)
Allergy symptoms in previous year (%)
Normal weight	20.0 (2.1)	1.00	1.00	18.6 (1.6)	1.00	1.00	.71
Overweight	17.1 (2.5)	0.83 (0.58-1.18)	0.85 (0.58-1.23)	19.2 (3.2)	0.94 (0.63-1.41)	1.05 (0.66-1.68)
Obese	17.4 (2.7)	0.85 (0.60-1.20)	0.90 (0.65-1.25)	16.7 (3.0)	0.82 (0.54-1.25)	0.90 (0.57-1.43)
Hay fever in previous year (%)
Normal weight	2.5 (0.7)	1.00	1.00	3.4 (1.4)	1.00	1.00	.73
Overweight	1.3 (1.2)	0.52 (0.05-4.99)	0.53 (0.05-5.40)	2.7 (1.3)	0.78 (0.21-2.84)	0.82 (0.20-3.41)
Obese	2.3 (0.5)	0.92 (0.42-2.01)	0.95 (0.41-2.20)	4.8 (1.5)	1.43 (0.54-3.79)	1.74 (0.67-4.49)
Itchy rash in previous year (%)
Normal weight	6.0 (1.0)	1.00	1.00	5.9 (0.8)	1.00	1.00	.02
Overweight	4.4 (1.8)	0.77 (0.27-2.20)	0.82 (0.28-2.36)	12.3 (2.1)	2.28 (1.29-4.03)	2.35 (1.30-4.25)
Obese	8.4 (2.5)	1.60 (0.93-2.75)	1.88 (1.02-3.45)	7.4 (1.7)	1.28 (0.70-2.34)	1.18 (0.62-2.27)

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Table E3. 

ORs by age group and ethnicity for the association between BMI and atopy, both overall and stratified by sex

Stratum: Atopy (≥1 positive specific IgE measurement)	Overall	P value∗	Male subjects	P value∗	Female subjects	P value∗
All subjects		—
Overweight	1.23 (0.98-1.54)		1.16 (0.86-1.57)		1.31 (0.96-1.79)	.55
Obese	1.35 (1.09-1.65)		1.18 (0.81-1.74)		1.54 (1.27-1.86)	.27
Age
Overweight vs normal		.87		.90		.91
2-5	1.53 (0.75-3.12)		1.27 (0.57-2.84)		1.96 (0.63-6.17)
6-10	1.17 (0.59-2.31)		1.26 (0.60-2.64)		1.08 (0.37-3.17)
11-14	1.00 (0.56-1.77)		0.90 (0.51-1.59)		1.13 (0.52-2.44)
15-19	1.21 (0.82–1.78)		1.18 (0.49-2.85)		1.34 (0.79-2.25)
Obese vs normal		.13		.08		.67
2-5	2.58 (1.45-4.60)		4.74 (1.46-15.4)		1.39 (0.55-3.53)
6-10	1.03 (0.63-1.69)		0.82 (0.39-1.70)		1.35 (0.67-2.73)
11-14	1.20 (0.82-1.77)		1.12 (0.49-2.54)		1.35 (0.96-1.88)
15-19	1.28 (0.88–1.88)		0.88 (0.45-1.72)		1.94 (1.23-3.07)
Race/ethnicity
Overweight vs normal		.75		.28		.82
Non-Hispanic white	1.29 (0.97-1.72)		1.24 (0.86-1.80)		1.39 (0.82-2.37)
Non-Hispanic black	0.98 (0.68-1.43)		0.77 (0.59-1.02)		1.23 (0.63-2.40)
Mexican American	1.09 (0.70-1.70)		1.06 (0.58-1.96)		1.11 (0.71-1.74)
Other	1.36 (0.45-4.11)		1.43 (0.26-7.81)		1.23 (0.36-4.16)
Obese vs normal		.76		.16		.0004
Non-Hispanic white	1.28 (0.94-1.74)		0.98 (0.56-1.73)		1.73 (1.22-2.46)
Non-Hispanic black	1.41 (1.06-1.87)		1.01 (0.64-1.58)		1.85 (1.37-2.50)
Mexican American	1.38 (1.07-1.78)		1.64 (1.12-2.41)		1.09 (0.81-1.47)
Other	1.00 (0.50-2.00)		1.73 (1.00-2.97)		0.41 (0.16-1.04)

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