339
BIRTH 41:4 December 2014
Widespread Usage of Infant Formula in China: A Major Public Health Problem Li Tang, PhD, Andy H. Lee, PhD, Colin W. Binns, PhD, Yuxiong Yang, MPH, Yan Wu, MB, Yanxia Li, MB, and Liqian Qiu, PhD ABSTRACT: Background: The potential health risks of infant formula feeding are well
established. This study investigated the opinions and perceptions of mothers and recommendations by hospital staff with respect to infant formula usage in China. Methods: A cross-sectional survey of 726 mothers within 6 months postpartum and 241 hospital staff, using structured questionnaires, was conducted in Hangzhou and Shenzhen, China. Results: Overall, 474 of 726 (65.3%) infants aged within 6 months had consumed some infant formula. About 40.0 percent of mothers chose a hybrid brand of formula (manufactured in China but owned by a foreign company), over imported (< 32.0%) and domestic brands (< 28.0%), despite their higher level of confidence on the quality of imported brands. Perceived insufficient breastmilk production (86.2%) was the most common reason for giving infant formula, followed by return to work (24.6%). Of the 241 hospital staff, 97 (40.2%) gave no recommendation about infant formula brand for infants at any age. However, 47.2 percent of the remaining staff recommended a hybrid brand in combination with an imported and/or a domestic product. Conclusions: Perceptions by mothers and recommendations from hospital staff appear to contribute to the widespread usage of infant formula in China. It is important to ensure breastmilk substitutes are prescribed to Chinese infants strictly for medical reasons. Maternal education programs incorporating information on food safety issues and establishment of breastfeeding-friendly workplaces could curtail the common practice of formula feeding in China. (BIRTH 41:4 December 2014) Key words: breastfeeding, breastmilk, China, infant formula, milk scandal
The World Health Assembly adopted the International Code of Marketing of Breastmilk Substitutes in 1981 to promote and protect breastfeeding and reduce the impact of marketing for infant formula and other breastmilk substitutes (1). Infant formula feeding has been linked to increased incidence and severity of infectious diseases, such as diarrhea, respiratory tract infections, and acute otitis media. Elevated risks of sud-
den infant death syndrome and allergic diseases have also been indicated (2). Breastfeeding for infants has known long-term benefits (3), whereas formula feeding is associated with a high economic burden and increased health care costs (4). Despite these disadvantages, the rate of early introduction of infant formula remains high over the last decade in China, with infant formula given to 38–68 percent of newborns as their
Li Tang is a Research Fellow, School of Public Health, Curtin University, WA, Australia; Andy H. Lee is a Professor, School of Public Health, Curtin University, WA, Australia; Colin W. Binns is a Professor, School of Public Health, Curtin University, WA, Australia; Yuxiong Yang is a Research Assistant, School of Public Health, Curtin University, WA, Australia; Yan Wu is a medical doctor, Yongkang Maternal and Children’s Hospital, Zhejiang, China; Yanxia Li is a medical doctor, Jiaxing Maternal and Children’s Hospital, Zhejiang, China; Liqian Qiu is a Professor, Women’s Hospital, Zhejiang University, Zhejiang, China.
Address correspondence to Andy H. Lee, School of Public Health, Curtin University, GPO Box U 1987, Perth, WA, 6845, Australia.
Accepted August 4, 2014
© 2014 Wiley Periodicals, Inc.
BIRTH 41:4 December 2014
340 first feed (5,6). Indeed, China is now the largest infant formula market in the world with a projected annual growth rate of 20 percent (7). Formula-fed infants are also exposed to additional health risks because of fake and contaminated products. A series of scandals concerning the additives or ingredients of infant formula have occurred in China during the past decade (8,9). In 2004, at least 13 Chinese infants died as a result of consuming fake infant formula (8). Four years later, the industrial chemical melamine was added to adulterate processed milk to give the appearance of attaining normal levels of protein (10). According to the World Health Organization, the melamine-contaminated milk powder and related dairy products caused at least 6 deaths, and more than 51,900 infants and young children were hospitalized with renal problems (11). These scandals have jeopardized Chinese parents’ trust in domestically manufactured infant formula and resulted in panic buying of foreign brands from overseas, causing a shortage in neighboring countries (8). Often, infant formula marketing is aggressive to the extent of violating the International Code of Marketing of Breastmilk Substitutes. In 2013, the official China Central Television reported that payments were made by an infant formula company to induce hospital staff to recommend its brand to expectant mothers and mothers of newborn infants (12). The Chinese media similarly reported that free formula samples were distributed at maternity hospitals, including some that have been accredited as “baby-friendly” (13). There have been several reports in the lay press in response to the continuing infant formula crisis in China, but scientific investigation from the users’ perspective of the underlying issues remains lacking. This study provides the first comprehensive report on the current perceptions and preferences of mothers and recommendations by hospital staff about infant formula usage in China.
Methods A cross-sectional survey was conducted in Hangzhou and Shenzhen between October 2013 and February 2014. Hangzhou, with a population of 7 million, is the capital city of Zhejiang Province in Eastern China. Shenzhen is a special economic zone next to Hong Kong and a major financial center for Guangdong Province in Southern China. The population of Shenzhen was about 10.5 million in 2012. Four maternal and children’s hospitals and three community health centers were randomly selected in each city, with a total target sample size of 800 mothers and 250 hospital staff given our available resources.
The survey has two components. In the first part, mothers within 6 months postpartum were approached when they brought their infants to the chosen sites for immunization or regular checkup. Those who gave consent were interviewed face-to-face by a trained research assistant using a structured questionnaire. Information sought included sociodemographic and maternal characteristics, the brand and cost of infant formula used, reasons for their choice and confidence in different brands. An 11-point Likert scale was used to rate levels of confidence, ranging from 0 (totally not confident) through 10 (totally confident). Each interview took about 10 minutes to complete. In the second part of the survey, staff from the maternity department, newborn unit, and maternal and childcare clinic of the participating hospitals were invited to provide their recommendations concerning infant formula usage. To maintain anonymity, only basic information on gender, department, and position were collected using a self-administered questionnaire distributed to the relevant departments. Questions on infant formula were phrased in scenario contexts because of the sensitivity of the issue. For example, in relation to infants aged under 1 month: “Sometimes mothers who underwent caesarean section with complications or had given birth prematurely may delay or not initiate breastfeeding. Under such circumstances, what brand(s) of infant formula do you recommend for their newborns?” Two similar questions were posed for infants aged 1 to 3 months and above 3 months. Data were entered and analyzed using the SPSS package version 21 (IBM, Armonk, NY, USA). To facilitate analysis, the various brands of infant formula were grouped into three categories: domestic, hybrid and imported, based on their place of origin. “Domestic” brands are those owned by Chinese companies and manufactured locally in China. This definition also applies to infant formula produced by Sino-foreign joint ventures. If the owner is a foreign company, but the milk formula is manufactured in China, the brand is considered as “hybrid.” “Imported” brands are defined as those owned by a foreign company and manufactured wholly outside China. Besides descriptive statistics, chi-square tests of association were performed to compare characteristics and outcome variables between subgroups of interest. The study protocol was approved by the participating facilities and the Human Research Ethics Committee of the principal researcher’s institution (approval number SPH-53-2013), and conformed to the provisions of the Declaration of Helsinki. An information sheet explaining the project was given and read to the mothers before obtaining their verbal consent. All participants were informed about their right to withdraw from the interview without prejudice. For the staff survey, participants
341
BIRTH 41:4 December 2014
were assured of the confidentiality of the information provided with no linkage to the identity of staff.
Results Of the total 792 eligible mothers approached, 726 consented to participate (n = 360 in Hangzhou, n = 366 in Shenzhen), giving a response rate of 91.7 percent. Moreover, 241 (n = 139 in Hangzhou, n = 102 in Shenzhen) out of 304 eligible hospital staff (171 in Hangzhou and 133 in Shenzhen) took part in the staff survey, yielding an overall staff participation rate of 79.3 percent. Table 1 shows the maternal characteristics of the participating mothers. They were aged between 18 and 45 years (median 27 years). Approximately 97 percent of women had a gestation of more than 37 weeks and almost half the women had a cesarean. At the time of interview, the majority of infants (59.5%) were aged between 3 and 6 months. The infant male to female ratio was about 1.4:1, with 94 percent of birthweight within the normal range 2.5–3.9 kg. As expected, mothers in Shenzhen tended to be employed, have higher education level, and higher family income than their counterparts in Hangzhou. The distributions of demographics, such as maternal age and working status, in this survey are similar to those presented in recent studies conducted in Shenzhen and Zhejiang Province (14,15). For hospital staff participants, the majority were female (86.7%), and from the maternity department (71.9%). Distribution of staff positions were: 44 percent nurses, 42 percent doctors, 12 percent midwives, and 2 percent administrators. Overall, 474 of 726 (65.3%) infants aged within 6 months had consumed some infant formula by the time of interview. Among the 136 infants aged 6 months, 66.9 percent had been given formula. Table 2 compares infant formula brands used by mothers at 1 week, 1 month, 3 months, and 6 months postpartum. The chi-square test result showed no difference in the distribution of brands used across the infant age groups (p = 0.501). About 40.0 percent of mothers chose a hybrid brand over imported (< 32.0%) and domestic brands (< 28.0%). The median price paid was 240 (interquartile range 80) yuan per 900 g can ( 40 USD). When purchasing infant formula, “word of mouth” (23.2%), “brand” (21.8%), and “ingredients” (18.2%) were the main considerations given by the 474 infant formula users. Perceived insufficient breastmilk production (86.2%) was the most common reason for giving infant formula, followed by return to work (24.6%). Mothers placed a higher level of confidence on the quality of imported (mean 7.0, SD 1.8) than hybrid (mean 5.4, SD 2.1) and domestic brands (mean 4.7, SD 2.2).
Table 3 summarizes results of the staff survey. The staff recommendations appeared to be similar across different infant age groups (p = 0.902), although 97 Table 1. Maternal Mothers
Characteristics
Total (n = 726) %
Variables
of
Participating
Hangzhou (n = 360) %
Shenzhen (n = 366) %
20.8 48.9 30.3
23.0 48.6 28.4
68.3
57.7
31.7
42.3
65.8 6.1 28.1
41.8 18.3 39.9
47.5 35.7 16.8
29.3 38.0 32.7
3.1 96.9
3.3 96.7
53.1 46.9
47.8 52.2
54.7 45.3
61.2 38.8
1.7 92.8 5.6
0.8 95.1 4.1
Age (years) < 25 21.9 25–29 48.8 ≥ 30 29.3 Education‡ High school or 62.9 below College or 37.1 university , Employment§ * No job 53.4 Part-time 12.4 Full-time 34.2 , Monthly family income (yuan)§ † ≤ 6,000 38.1 6,001–10,000 36.9 > 10,000 25.0 Gestation (weeks) < 37 3.2 ≥ 37 96.8 Method of delivery Vaginal 50.4 Cesarean 49.6 Gender of infant Male 58.0 Female 42.0 Birthweight (grams) < 2,500 1.2 2,500–3,999 94.0 ≥ 4,000 4.8
*Data unavailable for 18 mothers from Hangzhou. †Data unavailable for 21 mothers from Hangzhou and 8 mothers from Shenzhen. ‡ p < 0.05, §p < 0.01.
Table 2. Infant Formula Brands Used at 1 Week, 1 Month, 3 Months, and 6 Months Postpartum
Age of infant
Domestic No. (%)
1 1 3 6
84 76 54 26
week month months months
(26.5) (26.8) (27.6) (32.1)
Hybrid No. (%) 151 117 83 30
(47.6) (41.2) (42.3) (37.0)
Imported No. (%) 82 91 59 25
(25.9) (32.0) (30.1) (30.9)
BIRTH 41:4 December 2014
342 Table 3. Recommendations of Infant Formula by Hospital Staff
Age of infant Recommendation*
< 1 month 1–3 months > 3 months No. (%) No. (%) No. (%)
None Domestic Hybrid Imported Don’t know
107 44 74 36 10
(44.4) (18.3) (30.7) (14.9) (4.2)
106 40 66 43 7
(44.0) (16.6) (27.4) (17.8) (2.9)
105 39 63 38 13
(43.6) (16.2) (26.1) (15.8) (5.4)
*Multiple answers allowed.
staff (40.2%) did not recommend any infant formula overall. However, 47.2 percent of the remaining staff recommended a hybrid brand in combination with an imported and/or a domestic product; followed by almost equal proportions (about 28.0%) favoring imported or domestic brands, whereas about 7.0 percent indicated no preference. Finally, subgroup analysis by recruitment city produced similar results which were omitted for brevity.
Dicussion The finding that the majority of mothers had administered milk formula to their infants by 6 months of age is consistent with previous breastfeeding studies in China (15,16). The two main reasons reported by mothers for using infant formula, inadequate breastmilk production and return to work, have been recognized as common breastfeeding obstacles (17). This study confirmed the common belief that Chinese mothers have more confidence in the quality of imported brands of infant formula than domestic and hybrid products. However, in terms of actual purchase, they chose the hybrid brands and their preference appeared to be partially driven by the recommendations from hospital staff. To the best of our knowledge, no scientific study has been published that investigates the preferences and confidence of Chinese mothers or recommendations of hospital staff concerning infant formula usage. All previous reports on the topic came from the lay press. The few publications in the literature focused on the adverse health outcomes including deaths after exposure to fake or contaminated formula (8,11,18). Despite the series of scandals over the past decade, the consumption of infant formula remains widespread in China, which is a major public health problem. As part of its adoption of the Baby-friendly Hospital Initiative, the Chinese government introduced the “Marketing of Breastmilk Substitutes Management
Measures” as a national law in 1995. It follows most of the provisions in the International Code of Marketing of Breastmilk Substitutes, including absolutely no promotion of breastmilk substitutes within health facilities or by health professionals (19). Nevertheless, 60 percent of the staff surveyed recommended infant formula under certain provisions. Breastmilk substitutes should be prescribed to infants strictly for medical reasons (20). Besides “word of mouth,” “brand” and “ingredients of formula” were popular reasons affecting the mothers’ preferences, which may be related to aggressive marketing by formula companies. It is alarming yet easy to find advertisements in the media promoting the so-called health benefits of infant formula. Such misleading information not only influences a mother’s choice on brand but also her decision not to breastfeed (21). It is known that “safe” formula feeding depends on several requirements, including a safe water supply, correct dosage used, continued ability to purchase formula, effective refrigeration, and clean environments (22). The food safety issues should be incorporated into maternal education programs, aside from emphasizing the potential health hazards of formula consumption. Perceived “inadequate breastmilk production” and “return to work” were the main reasons provided by the mothers to justify their formula feeding. In fact, only 1–5 percent of women have genuine physiological problems with milk supply, whereas the vast majority can produce more than enough milk for their newborns (23). Sucking at the breast is known to stimulate milk production, whereas formula feeding, especially in the early months, can offset the continuous breastmilk supply. More importantly, full support should be given to new mothers immediately after delivery to establish successful breastfeeding, thus minimizing or even preventing the use of formula. To overcome the barrier of return to work, prolonging the maternity leave period can be an effective option (24). However, a realistic alternative may be legislating the work environment to be more breastfeeding-friendly, such as provision of flexible work schedules, breastfeeding breaks, and private rooms for lactating mothers. Major strengths of this study are the high response rates of our participants and the use of face-to-face interviews for the mothers’ survey. The convenience sampling method may pose some limitations in terms of selection bias. China is a large country with its cities in various stages of economic development. Our findings may not necessarily be generalized to the entire population particularly those residing in rural areas. Further studies with stringent sample selection, conducted in both urban and rural China, would provide more insights to the reasons and factors underlying the widespread usage of infant formula.
343
BIRTH 41:4 December 2014
Acknowledgment We are grateful to the mothers and hospital staff who participated in our survey.
13.
14.
References 1. World Health Organization. International Code of Marketing of Breast-Milk Substitutes. Geneva: World Health Organization, 1981:4–8. 2. American Academy of Pediatrics, Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics. 2012; 129(3):e827–e841. doi: http://dx.doi.org/10.1542/peds.2011-3552. 3. World Health Organization. Long-Term Effects of Breastfeeding: A Systematic Review. Geneva: World Health Organization, 2013. 4. Bartick M, Reinhold A. The burden of suboptimal breastfeeding in the United States: A pediatric cost analysis. Pediatrics 2010;125(5):e1048–e1056. 5. Tang L, Binns CW, Lee AH, et al. Low Prevalence of Breastfeeding Initiation within the First Hour of Life in a Rural Area of Sichuan Province, China. Birth 2013;40(2):134–142. 6. Tang L, Hewitt K, Yu C. Prelacteal feeds in China. Curr Pediatr Rev 2012;8(4):304–312. 7. UBIC Consulting. Ingredients for the world infant formula market. 2014. Accessed April 30, 2014. Available at: http://www. ubic-consulting.com/template/fs/documents/Nutraceuticals/Ingredients-in-the-world-infant-formula-market.pdf. 8. Ji AL, Wong YL, Cai TJ, Liu J. Infant formula safety concerns and consequences in China. World J Pediatr 2014;10(1):7–9. 9. Hon KL, Leung TF. Issues associated with formula milk: The Hong Kong’s experience. World J Pediatr 2014;10(1):5–6. 10. Parry J. China’s tainted milk scandal spreads around world. BMJ 2008;337:a1890. 11. World Health Organization. Toxicological and Health Aspects of Melamine and Cyanuric Acid: Report of a WHO Expert Meeting in Collaboration With FAO, Supported by Health Canada, Ottawa, Canada, 1–4 December 2008. Geneva: World Health Organization, 2009:1. 12. Zhao X, Peng Y, Yang Y. Bribery claims feed milk scandal. China Daily; 22 October 2013. Accessed April 22, 2014. Avail-
15.
16.
17.
18. 19.
20.
21.
22.
23.
24.
able at: http://usa.chinadaily.com.cn/china/2013-10/22/content_ 17049396.htm. Distribution of free formula in hospitals: the regulation is violated [in Chinese]. Peninsula City News; 2 Novermber 2011. Accessed April 22, 2014. Available at: http://qingdao.dzwww. com/xinwen/qingdaonews/201111/t20111102_6737719.htm. Luo YL, Cheng YL, Gao XH, et al. Maternal age, parity and isolated birth defects: A population-based case-control study in Shenzhen, China. PLoS ONE 2013;8(11):e81369. doi: 10.1371/ journal.pone.0081369 Qiu L, Binns CW, Zhao Y, et al. Breastfeeding practice in Zhejiang province, PR China, in the context of melamine-contaminated formula milk. J Health Popul Nutr 2010;28(2):189–198. Xu F, Binns C, Wu J, et al. Infant feeding practices in Xinjiang Uygur Autonomous Region, People’s Republic of China. Public Health Nutr 2007;10(2):198–202. Xu F, Qiu L, Binns CW, Liu X. Breastfeeding in China: A review. Int Breastfeed J 2009;4:6. doi: http://dx.doi.org/10.1186/ 1746-4358-4-6. Parry J. China’s tainted infant formula sickens nearly 13,000 babies. BMJ 2008;337:a1802. Ministry of Health of the People’s Republic of China. Marketing of Breastmilk Substitutes Management Measures [in Chinese]. Beijing: Ministry of Health of the People’s Republic of China; 2005. Accessed April 12, 2014. Available at: http://www.gov.cn/ banshi/2005-08/23/content_25511.htm. World Health Organization, UNICEF. Acceptable medical reasons for use of breast-milk substitutes. Geneva: World Health Organization, 2009:7–9. Stang J, Hoss K, Story M. Health statements made in infant formula advertisements in pregnancy and early parenting magazines: A content analysis. Infant Child Adolesc Nutr 2010;2(1):16–25. National Health and Medical Research Council. Infant Feeding Guidelines. Canberra: National Health and Medical Research Council, 2012:73–80. Inch S, Renfrew MJ. Common breastfeeding problems. In: Chalmers I, Enkin M, Keirse MJN, eds. Effective care in pregnancy and childbirth, Vol 1. Oxford: Oxford University Press, 1989:1377–1378. Ogbuanu C, Glover S, Probst J, et al. The effect of maternity leave length and time of return to work on breastfeeding. Pediatrics 2011;127(6):e1414–e1427.
Copyright of Birth: Issues in Perinatal Care is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
BIRTH 41:4 December 2014
Widespread Usage of Infant Formula in China: A Major Public Health Problem Li Tang, PhD, Andy H. Lee, PhD, Colin W. Binns, PhD, Yuxiong Yang, MPH, Yan Wu, MB, Yanxia Li, MB, and Liqian Qiu, PhD ABSTRACT: Background: The potential health risks of infant formula feeding are well
established. This study investigated the opinions and perceptions of mothers and recommendations by hospital staff with respect to infant formula usage in China. Methods: A cross-sectional survey of 726 mothers within 6 months postpartum and 241 hospital staff, using structured questionnaires, was conducted in Hangzhou and Shenzhen, China. Results: Overall, 474 of 726 (65.3%) infants aged within 6 months had consumed some infant formula. About 40.0 percent of mothers chose a hybrid brand of formula (manufactured in China but owned by a foreign company), over imported (< 32.0%) and domestic brands (< 28.0%), despite their higher level of confidence on the quality of imported brands. Perceived insufficient breastmilk production (86.2%) was the most common reason for giving infant formula, followed by return to work (24.6%). Of the 241 hospital staff, 97 (40.2%) gave no recommendation about infant formula brand for infants at any age. However, 47.2 percent of the remaining staff recommended a hybrid brand in combination with an imported and/or a domestic product. Conclusions: Perceptions by mothers and recommendations from hospital staff appear to contribute to the widespread usage of infant formula in China. It is important to ensure breastmilk substitutes are prescribed to Chinese infants strictly for medical reasons. Maternal education programs incorporating information on food safety issues and establishment of breastfeeding-friendly workplaces could curtail the common practice of formula feeding in China. (BIRTH 41:4 December 2014) Key words: breastfeeding, breastmilk, China, infant formula, milk scandal
The World Health Assembly adopted the International Code of Marketing of Breastmilk Substitutes in 1981 to promote and protect breastfeeding and reduce the impact of marketing for infant formula and other breastmilk substitutes (1). Infant formula feeding has been linked to increased incidence and severity of infectious diseases, such as diarrhea, respiratory tract infections, and acute otitis media. Elevated risks of sud-
den infant death syndrome and allergic diseases have also been indicated (2). Breastfeeding for infants has known long-term benefits (3), whereas formula feeding is associated with a high economic burden and increased health care costs (4). Despite these disadvantages, the rate of early introduction of infant formula remains high over the last decade in China, with infant formula given to 38–68 percent of newborns as their
Li Tang is a Research Fellow, School of Public Health, Curtin University, WA, Australia; Andy H. Lee is a Professor, School of Public Health, Curtin University, WA, Australia; Colin W. Binns is a Professor, School of Public Health, Curtin University, WA, Australia; Yuxiong Yang is a Research Assistant, School of Public Health, Curtin University, WA, Australia; Yan Wu is a medical doctor, Yongkang Maternal and Children’s Hospital, Zhejiang, China; Yanxia Li is a medical doctor, Jiaxing Maternal and Children’s Hospital, Zhejiang, China; Liqian Qiu is a Professor, Women’s Hospital, Zhejiang University, Zhejiang, China.
Address correspondence to Andy H. Lee, School of Public Health, Curtin University, GPO Box U 1987, Perth, WA, 6845, Australia.
Accepted August 4, 2014
© 2014 Wiley Periodicals, Inc.
BIRTH 41:4 December 2014
340 first feed (5,6). Indeed, China is now the largest infant formula market in the world with a projected annual growth rate of 20 percent (7). Formula-fed infants are also exposed to additional health risks because of fake and contaminated products. A series of scandals concerning the additives or ingredients of infant formula have occurred in China during the past decade (8,9). In 2004, at least 13 Chinese infants died as a result of consuming fake infant formula (8). Four years later, the industrial chemical melamine was added to adulterate processed milk to give the appearance of attaining normal levels of protein (10). According to the World Health Organization, the melamine-contaminated milk powder and related dairy products caused at least 6 deaths, and more than 51,900 infants and young children were hospitalized with renal problems (11). These scandals have jeopardized Chinese parents’ trust in domestically manufactured infant formula and resulted in panic buying of foreign brands from overseas, causing a shortage in neighboring countries (8). Often, infant formula marketing is aggressive to the extent of violating the International Code of Marketing of Breastmilk Substitutes. In 2013, the official China Central Television reported that payments were made by an infant formula company to induce hospital staff to recommend its brand to expectant mothers and mothers of newborn infants (12). The Chinese media similarly reported that free formula samples were distributed at maternity hospitals, including some that have been accredited as “baby-friendly” (13). There have been several reports in the lay press in response to the continuing infant formula crisis in China, but scientific investigation from the users’ perspective of the underlying issues remains lacking. This study provides the first comprehensive report on the current perceptions and preferences of mothers and recommendations by hospital staff about infant formula usage in China.
Methods A cross-sectional survey was conducted in Hangzhou and Shenzhen between October 2013 and February 2014. Hangzhou, with a population of 7 million, is the capital city of Zhejiang Province in Eastern China. Shenzhen is a special economic zone next to Hong Kong and a major financial center for Guangdong Province in Southern China. The population of Shenzhen was about 10.5 million in 2012. Four maternal and children’s hospitals and three community health centers were randomly selected in each city, with a total target sample size of 800 mothers and 250 hospital staff given our available resources.
The survey has two components. In the first part, mothers within 6 months postpartum were approached when they brought their infants to the chosen sites for immunization or regular checkup. Those who gave consent were interviewed face-to-face by a trained research assistant using a structured questionnaire. Information sought included sociodemographic and maternal characteristics, the brand and cost of infant formula used, reasons for their choice and confidence in different brands. An 11-point Likert scale was used to rate levels of confidence, ranging from 0 (totally not confident) through 10 (totally confident). Each interview took about 10 minutes to complete. In the second part of the survey, staff from the maternity department, newborn unit, and maternal and childcare clinic of the participating hospitals were invited to provide their recommendations concerning infant formula usage. To maintain anonymity, only basic information on gender, department, and position were collected using a self-administered questionnaire distributed to the relevant departments. Questions on infant formula were phrased in scenario contexts because of the sensitivity of the issue. For example, in relation to infants aged under 1 month: “Sometimes mothers who underwent caesarean section with complications or had given birth prematurely may delay or not initiate breastfeeding. Under such circumstances, what brand(s) of infant formula do you recommend for their newborns?” Two similar questions were posed for infants aged 1 to 3 months and above 3 months. Data were entered and analyzed using the SPSS package version 21 (IBM, Armonk, NY, USA). To facilitate analysis, the various brands of infant formula were grouped into three categories: domestic, hybrid and imported, based on their place of origin. “Domestic” brands are those owned by Chinese companies and manufactured locally in China. This definition also applies to infant formula produced by Sino-foreign joint ventures. If the owner is a foreign company, but the milk formula is manufactured in China, the brand is considered as “hybrid.” “Imported” brands are defined as those owned by a foreign company and manufactured wholly outside China. Besides descriptive statistics, chi-square tests of association were performed to compare characteristics and outcome variables between subgroups of interest. The study protocol was approved by the participating facilities and the Human Research Ethics Committee of the principal researcher’s institution (approval number SPH-53-2013), and conformed to the provisions of the Declaration of Helsinki. An information sheet explaining the project was given and read to the mothers before obtaining their verbal consent. All participants were informed about their right to withdraw from the interview without prejudice. For the staff survey, participants
341
BIRTH 41:4 December 2014
were assured of the confidentiality of the information provided with no linkage to the identity of staff.
Results Of the total 792 eligible mothers approached, 726 consented to participate (n = 360 in Hangzhou, n = 366 in Shenzhen), giving a response rate of 91.7 percent. Moreover, 241 (n = 139 in Hangzhou, n = 102 in Shenzhen) out of 304 eligible hospital staff (171 in Hangzhou and 133 in Shenzhen) took part in the staff survey, yielding an overall staff participation rate of 79.3 percent. Table 1 shows the maternal characteristics of the participating mothers. They were aged between 18 and 45 years (median 27 years). Approximately 97 percent of women had a gestation of more than 37 weeks and almost half the women had a cesarean. At the time of interview, the majority of infants (59.5%) were aged between 3 and 6 months. The infant male to female ratio was about 1.4:1, with 94 percent of birthweight within the normal range 2.5–3.9 kg. As expected, mothers in Shenzhen tended to be employed, have higher education level, and higher family income than their counterparts in Hangzhou. The distributions of demographics, such as maternal age and working status, in this survey are similar to those presented in recent studies conducted in Shenzhen and Zhejiang Province (14,15). For hospital staff participants, the majority were female (86.7%), and from the maternity department (71.9%). Distribution of staff positions were: 44 percent nurses, 42 percent doctors, 12 percent midwives, and 2 percent administrators. Overall, 474 of 726 (65.3%) infants aged within 6 months had consumed some infant formula by the time of interview. Among the 136 infants aged 6 months, 66.9 percent had been given formula. Table 2 compares infant formula brands used by mothers at 1 week, 1 month, 3 months, and 6 months postpartum. The chi-square test result showed no difference in the distribution of brands used across the infant age groups (p = 0.501). About 40.0 percent of mothers chose a hybrid brand over imported (< 32.0%) and domestic brands (< 28.0%). The median price paid was 240 (interquartile range 80) yuan per 900 g can ( 40 USD). When purchasing infant formula, “word of mouth” (23.2%), “brand” (21.8%), and “ingredients” (18.2%) were the main considerations given by the 474 infant formula users. Perceived insufficient breastmilk production (86.2%) was the most common reason for giving infant formula, followed by return to work (24.6%). Mothers placed a higher level of confidence on the quality of imported (mean 7.0, SD 1.8) than hybrid (mean 5.4, SD 2.1) and domestic brands (mean 4.7, SD 2.2).
Table 3 summarizes results of the staff survey. The staff recommendations appeared to be similar across different infant age groups (p = 0.902), although 97 Table 1. Maternal Mothers
Characteristics
Total (n = 726) %
Variables
of
Participating
Hangzhou (n = 360) %
Shenzhen (n = 366) %
20.8 48.9 30.3
23.0 48.6 28.4
68.3
57.7
31.7
42.3
65.8 6.1 28.1
41.8 18.3 39.9
47.5 35.7 16.8
29.3 38.0 32.7
3.1 96.9
3.3 96.7
53.1 46.9
47.8 52.2
54.7 45.3
61.2 38.8
1.7 92.8 5.6
0.8 95.1 4.1
Age (years) < 25 21.9 25–29 48.8 ≥ 30 29.3 Education‡ High school or 62.9 below College or 37.1 university , Employment§ * No job 53.4 Part-time 12.4 Full-time 34.2 , Monthly family income (yuan)§ † ≤ 6,000 38.1 6,001–10,000 36.9 > 10,000 25.0 Gestation (weeks) < 37 3.2 ≥ 37 96.8 Method of delivery Vaginal 50.4 Cesarean 49.6 Gender of infant Male 58.0 Female 42.0 Birthweight (grams) < 2,500 1.2 2,500–3,999 94.0 ≥ 4,000 4.8
*Data unavailable for 18 mothers from Hangzhou. †Data unavailable for 21 mothers from Hangzhou and 8 mothers from Shenzhen. ‡ p < 0.05, §p < 0.01.
Table 2. Infant Formula Brands Used at 1 Week, 1 Month, 3 Months, and 6 Months Postpartum
Age of infant
Domestic No. (%)
1 1 3 6
84 76 54 26
week month months months
(26.5) (26.8) (27.6) (32.1)
Hybrid No. (%) 151 117 83 30
(47.6) (41.2) (42.3) (37.0)
Imported No. (%) 82 91 59 25
(25.9) (32.0) (30.1) (30.9)
BIRTH 41:4 December 2014
342 Table 3. Recommendations of Infant Formula by Hospital Staff
Age of infant Recommendation*
< 1 month 1–3 months > 3 months No. (%) No. (%) No. (%)
None Domestic Hybrid Imported Don’t know
107 44 74 36 10
(44.4) (18.3) (30.7) (14.9) (4.2)
106 40 66 43 7
(44.0) (16.6) (27.4) (17.8) (2.9)
105 39 63 38 13
(43.6) (16.2) (26.1) (15.8) (5.4)
*Multiple answers allowed.
staff (40.2%) did not recommend any infant formula overall. However, 47.2 percent of the remaining staff recommended a hybrid brand in combination with an imported and/or a domestic product; followed by almost equal proportions (about 28.0%) favoring imported or domestic brands, whereas about 7.0 percent indicated no preference. Finally, subgroup analysis by recruitment city produced similar results which were omitted for brevity.
Dicussion The finding that the majority of mothers had administered milk formula to their infants by 6 months of age is consistent with previous breastfeeding studies in China (15,16). The two main reasons reported by mothers for using infant formula, inadequate breastmilk production and return to work, have been recognized as common breastfeeding obstacles (17). This study confirmed the common belief that Chinese mothers have more confidence in the quality of imported brands of infant formula than domestic and hybrid products. However, in terms of actual purchase, they chose the hybrid brands and their preference appeared to be partially driven by the recommendations from hospital staff. To the best of our knowledge, no scientific study has been published that investigates the preferences and confidence of Chinese mothers or recommendations of hospital staff concerning infant formula usage. All previous reports on the topic came from the lay press. The few publications in the literature focused on the adverse health outcomes including deaths after exposure to fake or contaminated formula (8,11,18). Despite the series of scandals over the past decade, the consumption of infant formula remains widespread in China, which is a major public health problem. As part of its adoption of the Baby-friendly Hospital Initiative, the Chinese government introduced the “Marketing of Breastmilk Substitutes Management
Measures” as a national law in 1995. It follows most of the provisions in the International Code of Marketing of Breastmilk Substitutes, including absolutely no promotion of breastmilk substitutes within health facilities or by health professionals (19). Nevertheless, 60 percent of the staff surveyed recommended infant formula under certain provisions. Breastmilk substitutes should be prescribed to infants strictly for medical reasons (20). Besides “word of mouth,” “brand” and “ingredients of formula” were popular reasons affecting the mothers’ preferences, which may be related to aggressive marketing by formula companies. It is alarming yet easy to find advertisements in the media promoting the so-called health benefits of infant formula. Such misleading information not only influences a mother’s choice on brand but also her decision not to breastfeed (21). It is known that “safe” formula feeding depends on several requirements, including a safe water supply, correct dosage used, continued ability to purchase formula, effective refrigeration, and clean environments (22). The food safety issues should be incorporated into maternal education programs, aside from emphasizing the potential health hazards of formula consumption. Perceived “inadequate breastmilk production” and “return to work” were the main reasons provided by the mothers to justify their formula feeding. In fact, only 1–5 percent of women have genuine physiological problems with milk supply, whereas the vast majority can produce more than enough milk for their newborns (23). Sucking at the breast is known to stimulate milk production, whereas formula feeding, especially in the early months, can offset the continuous breastmilk supply. More importantly, full support should be given to new mothers immediately after delivery to establish successful breastfeeding, thus minimizing or even preventing the use of formula. To overcome the barrier of return to work, prolonging the maternity leave period can be an effective option (24). However, a realistic alternative may be legislating the work environment to be more breastfeeding-friendly, such as provision of flexible work schedules, breastfeeding breaks, and private rooms for lactating mothers. Major strengths of this study are the high response rates of our participants and the use of face-to-face interviews for the mothers’ survey. The convenience sampling method may pose some limitations in terms of selection bias. China is a large country with its cities in various stages of economic development. Our findings may not necessarily be generalized to the entire population particularly those residing in rural areas. Further studies with stringent sample selection, conducted in both urban and rural China, would provide more insights to the reasons and factors underlying the widespread usage of infant formula.
343
BIRTH 41:4 December 2014
Acknowledgment We are grateful to the mothers and hospital staff who participated in our survey.
13.
14.
References 1. World Health Organization. International Code of Marketing of Breast-Milk Substitutes. Geneva: World Health Organization, 1981:4–8. 2. American Academy of Pediatrics, Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics. 2012; 129(3):e827–e841. doi: http://dx.doi.org/10.1542/peds.2011-3552. 3. World Health Organization. Long-Term Effects of Breastfeeding: A Systematic Review. Geneva: World Health Organization, 2013. 4. Bartick M, Reinhold A. The burden of suboptimal breastfeeding in the United States: A pediatric cost analysis. Pediatrics 2010;125(5):e1048–e1056. 5. Tang L, Binns CW, Lee AH, et al. Low Prevalence of Breastfeeding Initiation within the First Hour of Life in a Rural Area of Sichuan Province, China. Birth 2013;40(2):134–142. 6. Tang L, Hewitt K, Yu C. Prelacteal feeds in China. Curr Pediatr Rev 2012;8(4):304–312. 7. UBIC Consulting. Ingredients for the world infant formula market. 2014. Accessed April 30, 2014. Available at: http://www. ubic-consulting.com/template/fs/documents/Nutraceuticals/Ingredients-in-the-world-infant-formula-market.pdf. 8. Ji AL, Wong YL, Cai TJ, Liu J. Infant formula safety concerns and consequences in China. World J Pediatr 2014;10(1):7–9. 9. Hon KL, Leung TF. Issues associated with formula milk: The Hong Kong’s experience. World J Pediatr 2014;10(1):5–6. 10. Parry J. China’s tainted milk scandal spreads around world. BMJ 2008;337:a1890. 11. World Health Organization. Toxicological and Health Aspects of Melamine and Cyanuric Acid: Report of a WHO Expert Meeting in Collaboration With FAO, Supported by Health Canada, Ottawa, Canada, 1–4 December 2008. Geneva: World Health Organization, 2009:1. 12. Zhao X, Peng Y, Yang Y. Bribery claims feed milk scandal. China Daily; 22 October 2013. Accessed April 22, 2014. Avail-
15.
16.
17.
18. 19.
20.
21.
22.
23.
24.
able at: http://usa.chinadaily.com.cn/china/2013-10/22/content_ 17049396.htm. Distribution of free formula in hospitals: the regulation is violated [in Chinese]. Peninsula City News; 2 Novermber 2011. Accessed April 22, 2014. Available at: http://qingdao.dzwww. com/xinwen/qingdaonews/201111/t20111102_6737719.htm. Luo YL, Cheng YL, Gao XH, et al. Maternal age, parity and isolated birth defects: A population-based case-control study in Shenzhen, China. PLoS ONE 2013;8(11):e81369. doi: 10.1371/ journal.pone.0081369 Qiu L, Binns CW, Zhao Y, et al. Breastfeeding practice in Zhejiang province, PR China, in the context of melamine-contaminated formula milk. J Health Popul Nutr 2010;28(2):189–198. Xu F, Binns C, Wu J, et al. Infant feeding practices in Xinjiang Uygur Autonomous Region, People’s Republic of China. Public Health Nutr 2007;10(2):198–202. Xu F, Qiu L, Binns CW, Liu X. Breastfeeding in China: A review. Int Breastfeed J 2009;4:6. doi: http://dx.doi.org/10.1186/ 1746-4358-4-6. Parry J. China’s tainted infant formula sickens nearly 13,000 babies. BMJ 2008;337:a1802. Ministry of Health of the People’s Republic of China. Marketing of Breastmilk Substitutes Management Measures [in Chinese]. Beijing: Ministry of Health of the People’s Republic of China; 2005. Accessed April 12, 2014. Available at: http://www.gov.cn/ banshi/2005-08/23/content_25511.htm. World Health Organization, UNICEF. Acceptable medical reasons for use of breast-milk substitutes. Geneva: World Health Organization, 2009:7–9. Stang J, Hoss K, Story M. Health statements made in infant formula advertisements in pregnancy and early parenting magazines: A content analysis. Infant Child Adolesc Nutr 2010;2(1):16–25. National Health and Medical Research Council. Infant Feeding Guidelines. Canberra: National Health and Medical Research Council, 2012:73–80. Inch S, Renfrew MJ. Common breastfeeding problems. In: Chalmers I, Enkin M, Keirse MJN, eds. Effective care in pregnancy and childbirth, Vol 1. Oxford: Oxford University Press, 1989:1377–1378. Ogbuanu C, Glover S, Probst J, et al. The effect of maternity leave length and time of return to work on breastfeeding. Pediatrics 2011;127(6):e1414–e1427.
Copyright of Birth: Issues in Perinatal Care is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
