Atopic disorders, predominantly eczema and atopic dermatitis, affected up to 15 percent of Hong Kong children aged 14 and under in 2011 [1
]. This is comparable to the rates reported in most Western countries, ranging from 12.5 to 23.4 percent [2
], and much lower than the 25 to 40 percent reported in Australia [5
Atopic manifestations are not apparent at birth, but usually appear in early infancy, before the age of three months. That the etiology of atopic manifestations involves both heredity and the environment has been well documented. An individual with one parent and a sibling with a history of atopic illness has a 40% chance of developing an atopic illness [5
]. The environmental determinant includes everything surrounding a child, including the child’s birthplace, home, playmates, and diet. A number of benign items from the environment such as dust, pets, pollen, and so forth, have been recognized as allergens that, with contact, could lead to the manifestation of atopic illness in children. Studies have identified exposure to carpeting [6
], preschool [7
], dust mites [5
], pets [8
], antibiotic use in the prenatal period or in childhood [9
], siblings [10
], and the first exposure to solid food [12
] as factors associated with atopic manifestations. Besides heredity and the environment, there is growing evidence that some approaches to feeding in early life are associated with the development of atopic illness.
It is well accepted that breast milk provides optimal nourishment for neonates and protection against infection and allergies [14
]. Breast milk offers passive immunity to infants through secretory immunoglobulin A (IgA) antibodies that neutralize countless pathogenic microorganisms [15
]. Breast milk also contains probiotic substances that trigger the growth of a number of beneficial microflora in the gut of infants [17
]. It has been reported that breastfeeding (BF) for 3 weeks already enhances the effects of gut maturation in infants and provides protective factors against allergenic antigens [7
However, within the context of atopy, some researchers now consider long durations of exclusive breastfeeding (EBF) to be a contraindication rather than a preventative measure. Some studies have reported an increased risk of eczema or atopic dermatitis [18
] and asthma [21
] from prolonged EBF among children aged five and under. Specifically, the risk of atopic dermatitis increased with each added month of BF [18
], in circumstances of EBF for a duration of over 2 months [20
] or for a longer period of 6 months [19
A number of studies have claimed that there is no evidence to show that EBF has either a protective or harmful effect on atopic development in children [19
]. There is also an ongoing debate about the effect of the timing of the first exposure to solid food for toddlers in relation to the development of atopy. Parents are recommended to delay exposing their toddlers to solid or complementary foods until they reach the age of 6 months [24
]. However, there is recent evidence to suggest that the early introduction of solid foods is beneficial [12
]. In 2010, in a Finnish birth cohort study [12
], an increased incidence of atopy involving an allergic sensitization to food and inhalant allergens was observed of toddlers at age of five, and associated with the introduction of complementary foods at 4 months or later. The results of this study challenge the commonly recommended practice. In 2013, further evidence from the same study indicated that the risk of sensitization to various allergens was significantly reduced by the early introduction of complementary foods and the short duration of breastfeeding [13
]. Similar observations were reported on the development of eczema [25
Despite the debate, overall BF rates are on the decline globally. The rate at which BF is initiated is relatively high in most countries; however, there a significant decline in BF is seen the early months of infancy. In the United States, 74% of the mothers of all infants born in 2006 initiated BF, but EBF rates dropped to 34% and 14% by the ages of 3 and 6 months, respectively [27
]. In the United Kingdom, 69% of mothers initiated BF at birth, but 21% and 36% discontinued the practice within the first 2 and 6 weeks, respectively [28
]. In China, BF rates are higher than in Western countries, but vary between cities. The reported BF rates of cities from the northern to southern part of China from initiation to 4 months ranged from 54% and 37% in Beijing, 76.1% and 60.6% in Nanjing, and 94% and 56.6% in Guangzhou [29
]. In Hong Kong, the initiation rate of BF was shown to be 74% in hospitals, but the EBF rate dropped to 24.1% at 6 weeks postpartum
]. The public has been urged to increase breast feeding rates, with the argument that breast feeding offers optimal nutrition and natural protection to infants through antibodies passed on by the mother, and reduces the risk that the mother will develop breast cancer [31
A systematic review conducted in 2012 revealed a trend of increase in atopic eczema between 1990 and 2010 in young children globally, including in some parts of Asia [9
]. With the rise in atopy globally and with the controversy over the benefits of breast feeding and the early introduction of solid food in relation to atopy, there is a need to evaluate the evidence on the relationship between BF, the introduction of solid food, and atopic manifestations. Whether breast milk offers infants optimal immunity protection against atopy warrants investigation. The aim of this study is to explore the association between the type of feeding and the timing of the introduction of solid food, as well as maternal and prenatal confounding factors, family history, and environmental factors with the development of atopic illnesses in toddlers aged 4 months to 3 years.
2. Experimental Section
2.1. Study Design
This was a case-control study to examine the association between heredity, environment, and other confounding factors such as “type of feeding,” and atopic manifestations in toddlers aged 4 months to 3 years. The “cases” were toddlers with a medical diagnosis of atopy, while the “controls” were toddlers without atopy. The two groups of toddlers were compared in terms of their family history, environment, and types of feeding.
2.2. Subjects and Recruitment
The target population of this study was toddlers with or without atopy. The criteria for inclusion were toddlers between 4 months and 3 years of age who were born with no identifiable health issues, and who have or do not have atopy. Those who did not meet the inclusion criteria were excluded. Mothers with toddlers were recruited from the clinics of a private medical group in Hong Kong. This medical group has a total of three branches, which are located on Hong Kong Island, the south side of Hong Kong, and Lantau Island. The clinics provide pediatric health care services. Their clientele consists of mothers who bring their children in for scheduled check-ups or vaccinations, or to see a doctor if their child is unwell. The mothers were invited to join the study at the time of their visit.
All mothers with toddlers who fit the inclusion criteria were invited to participate in the study by completing a questionnaire on their child’s birth history, feeding mode, environmental exposure, family history, and atopic history. The mothers were given an explanation of the study and an information sheet on the study by a nurse working at the clinic. The mothers were clearly told that refusing to participate in the study would have no effect on the care that they receive from the clinic. Implied consent to participate in the study was given by those who agreed to complete the questionnaire developed for the study. A pediatrician in the clinic referred mothers of toddlers with known cases of atopy for participation in the study with a ticked box on the questionnaire to indicate the toddlers’ diagnosis of atopy. Known cases of atopy included diagnoses of eczema or allergic dermatitis, asthma, rhinitis, conjunctivitis (not related to infection), and allergies (dust mite, food, drug, etc.).
2.3. Development of the Questionnaire
A questionnaire was developed to solicit information on the birth history of the toddlers, the mother’s demographic data, the atopic history of the toddler and the toddler’s parents and siblings, and information on environmental factors. The questionnaire consisted of five sections:
- Section 1:
Birth history of the toddler, including gestational age, whether the toddler is singleton/twin, birth weight, and any health issue at birth (to confirm eligibility for inclusion);
- Section 2:
Mode of delivery (cesarean section or vaginal delivery), types of feeding (breast fed or formula fed, including duration; and introduction of solid food).
- Section 3:
Information on environmental factors, such as the history of maternal exposures, the hospitalization of the mother, maternal antibiotic use in utero or during breast feeding, the presence of siblings, carpets, pets, and so forth.
- Section 4:
Information on the parents’ atopic history, such as maternal self-reported or medically diagnosed allergic disease-atopic eczema, allergic rhinitis, asthma or food allergies, and so on.
- Section 5:
Information on the toddler’s atopic history, such as the occurrence of dermatological atopic manifestations, eczema, rhinitis, and other ailments, as well as history of hospitalization.
The questions in Sections 1 to 3 of the instrument were self-developed, based on a review of related literature. Section 4 consists of eight questions, which were modified from Lakwijk [33
] The 16 questions in Section 5 were modified from the International Study of Asthma and Allergies in children (ISAAC) study. Three questions modified from Kilpeläinen [34
] were added to this section.
The questionnaire went through a process of expert validation of the appropriateness and relevance of the questions. Five experts consisting of three pediatricians (one specializing in allergies) and two pediatric nurses were invited to validate the questionnaire. The content validity was calculated to be 0.91. A pilot test of the questionnaire was conducted among five mothers to determine whether they could understand the questions. The questionnaire was revised with larger bold font and wider spacing for easy reading. The mothers considered all of the questions to be comprehensible.
2.4. Data Processing and Analysis
The collected data were analyzed using SPSS Version 21.0 (IBM, Armonk, NY, USA). Descriptive statistics (frequency and percentages) were used to describe the demographics, characteristics of maternal and prenatal factors, environmental factors, and atopic manifestations of the toddlers. Toddlers were grouped according to those with a medical diagnosis of atopic disease and those without, and a statistical comparison was made of the toddlers’ demographic data and birth mode, the atopic history of their parents and siblings, environmental factors, and types of feeding. A t‑test was used to compare the parametric data, while all other nominal factors were compared using a chi-square test to determine statistical significance. Fisher’s exact test was used for groups with fewer than five subjects. All of the factors that had been identified as having statistical significance in relation to toddlers with atopic illness were included as independent variables in a logistic regression analysis performed to identify the contribution of factors of atopic illness in toddlers.
2.5. Ethical Consideration
Ethical approval was sought from the Human Subjects Ethics Sub-committee of The Hong Kong Polytechnic University. Mothers of toddlers were provided with a full explanation of the nature of the study, and it was confirmed that their participation was voluntary and that their non-participation would not affect the treatment received from physicians or nurses in the clinic. The completion of the questionnaire was considered a sign of implied consent. The participants were assured that their data would be kept confidential in accordance with the Privacy Ordinance. The anonymity of the individuals involved was ensured by the aggregation of statistical data. Access to the data was restricted to the researchers. Ethical approval was also sought and obtained from the governing body of the medical clinics, who were provided with copies of the research proposal and the questionnaire.