Conceived and designed the study: HB GE PK KS TDQ PP AH ES. Enrolled mothers and collected data: KS TDQ PP AH ES PK HB. Analyzed the data: HB GE. Wrote the manuscript: HB. Participated to the writing of the manuscript: GE KS TDQ PP AH ES PK.
The authors have declared that no competing interests exist.
Developing countries with traditionally breastfeeding are now experiencing the increasing pressure of formula milk marketing. This may endanger lives and undermine the efforts of national policies in achieving the objectives of the Millennium Development Goals. We examined the use of, and factors for use, of all available breast-milk substitutes (BMS) in a country with a traditionally high rate of breastfeeding.
Randomised multi-stage sampling surveys in 90 villages in 12/17 provinces in Laos.
Participants: 1057 mothers with infants under 24 months of age.
Tools: 50-query questionnaire and a poster of 22 BMS (8 canned or powdered milk; 6 non-dairy; 6 formulas; 2 non-formulas).
Outcome measures included: prevalence of use and age of starting BMS in relation to socio-demographic characteristics and information sources, by univariate and multivariate analyses.
Of 1057 mothers: 72.5% currently breastfed; 25.4% gave BMS (10.6% infant formula); 19.6% gave BMS before 6 months of age (of them: 83% non-dairy or cereals; mean age: 2.9 months; 95% Confidence interval: 2.6–3.2). One formula and one non-formula product accounted for 85% of BMS. BMS were considered as milk by the majority of mothers. Thai TV was the main source of information on BMS for mothers. Lao Loum mothers (the main ethnic group) living in concrete houses with good sanitary conditions, were more likely than others to use BMS before 6 months (OR: 1.79, (1.15–2.78), p<0.009). Mothers who fed their infants colostrum at birth were less likely to use BMS before 6 months of age (OR: 0.63, (0.41–0.99), p = 0.04). Unemployed mothers living in rural areas were less likely to consider BMS better than breast milk.
In Laos, mothers with the highest socio-economic status are showing a tendency to give up breastfeeding. Successful educational strategies and advocacy measures should be urgently developed to promote and sustain breastfeeding in developing countries.
Exclusive breastfeeding (EBF), an essential intervention to improve child survival
For many years, it has been recognized that in unhygienic conditions breast-milk substitutes carry a higher risk of infection than breastfeeding and can be fatal for infants
Depriving infants and mothers of the benefits of breastfeeding is challenging all 8 Millennium Development Goals (MDGs)
The attractiveness of BMS is of concern in low income countries as these products become increasingly available
Laos is a multi-ethnic and multilingual country with more than 45 languages. The official literacy rate (73%) does not reflect the disparity between the urban (89%) and rural areas (54%)
Inadequate breastfeeding and weaning practices contribute to high rates of malnutrition and infant and child mortality
We previously reported the misleading impact of a label on a coffee creamer which showed a bear suckling its cub. This resulted in 18% Lao mothers giving this creamer to their infants from the average age of 4.7 months in 2007
In this current survey we assess the prevalence of, and factors influencing, the use of BMS for Lao children less than 6 months of age. This survey is the first study to examine the use of BMS nationwide in a developing country.
Of the 16 provinces representing the geographical strata of Laos (North: from Phongsaly to Xayaboury, Luang Prabang and Xieng Khuang, Central (Vientiane and Borikhamxay), South (from Khammuan to Champassak) 12 were selected, based on the influence of bordering countries (China, Vietnam, and Thailand) (
Rural and urban areas were defined by the Lao government in the National Housing Census 2005
A 50-query questionnaire examined the mothers' knowledge and usage of BMS available in Laos. Mothers were shown a poster with the pictures of 22 different BMS (
Data collection was conducted from 1 March to 4 April 2009. Investigators were students of the Institut de la Francophonie pour la Médecine Tropicale (IFMT, Vientiane, Laos) who were young doctors attending a 2-year master's course with special lectures on Epidemiology, Field Research and Public Health. They were fluent in some of the languages used in the different areas. They were trained in interview techniques prior to the field survey. Local facilitators fluent in Lao were used when needed.
Main outcome measure was the prevalence of use, and age of starting BMS. Secondary outcomes were: knowledge of BMS and source of information on BMS; rate of BMS use before 6 months of age; reasons for use of BMS and its cost; rate of current breastfeeding; rate of breastfeeding within 24 hours; and EBF among infants 5–6 months.
Inappropriate breast-milk substitutes (IBMS) use was defined as the use of any of the BMS before the age of 6 months. EBF was estimated using the characteristics of breastfeeding the day before the interview. Breastfeeding (BF) was defined as EBF if the mother complied with 4 criteria: baby received BF the day before; baby did not receive any solid food; baby did not receive any other liquid or semi-liquid food.
Using Stata Version 8 (Stata Cooperation, College Station, TX), we calculated a necessary sample size of 1040 people based on an estimated 40% use of canned or fresh milk for infants in Lao reproductive health survey
Data was double entered with Epidata (
The survey was done in compliance with the Helsinki Declaration
Of 1057 mothers, 34.6% lived in urban areas, 42% belonged to ethnic minorities, 20% were illiterate and only 53% could speak Lao.
Urban | Rural | Total | ||
366 (34.6%) | 691 (65.4%) |
|
1057 (100%) | |
Age (years) |
27.7 (27–28.4) | 25.6 (25.1–26) | 0.000 | 26.3 (26–27) |
Ethnic Group | ||||
- Lao Loum |
294 (80.3) | 281 (40.7) | 0.000 | 575 (54.4) |
- Lao Theung |
29 (7.9) | 174 (25.2) | 203 (19.2) | |
- Lao Soung |
41 (11.2) | 200 (28.9) | 241 (22.8) | |
Illiterate | 25 (6.8) | 185 (26.8) | 0.000 | 210 (19.9) |
Can speak Lao | 282 (77.1) | 279 (40.4) | 0.000 | 561 (53.1) |
Husband illiterate | 20 (5.5) | 119 (17.2) | <0.000 | 139 (13.2) |
Farmers |
112(30.6) | 538(77.9) | <0.000 | 650(61.5) |
Number of children |
2 (1.9–2.2) | 2.5 (2.4–2.7) | <0.000 | 2.35 (2.3–2.6) |
Ante-natal care |
326 (89.1) | 467 (67.6) | 0.000 | 793 (75.0) |
Daily expenses for food |
4.5 (4–5) | 1.92 (1.8–2) | <0.000 | 2.8 (2.6–3) |
Availability of tap water | 277 (75.7) | 382 (55.3) | 0.000 | 659 (62.4) |
Latrines | 303 (82.8) | 434 (64.8) | 0.000 | 737 (69.7) |
No electricity | 17 (4.6) | 254 (36.8) | <0.000 | 271 (25.6) |
Have a TV | 313 (90.2) | 309(58.9) | 0.000 | 622 (71.3) |
Have a radio | 78 (21.3) | 122 (17.6) | 0.1 | 200 (18.9) |
*mean (95% confidence interval);
**This classification is used to roughly describe ethnic groups belonging to lowlands, midlands and highlands though people may have migrated since then from their original residency.
834 (78.9%) reported an occupation: 73 (6.9%) civil servants, 60 (5.7%) shop keepers, 18 (1.7%) workers, 16 (1.5%) other occupations.
At list one visit.
In US dollars: US = 8000 Lao kip.
Urban | Rural | Total | ||
366 (34.6%) | 691 (65.4%) |
|
1057 (100%) | |
Sex (Male) | 188 (51.4) | 364 (52.9) | 0.7 | 552 (52.2) |
Age (Months) |
11.5 (10.7–12.3) | 11.7 (11.2–12.3) | 0.3 | 11.64 (11.2–112) |
- 0–6months | 122 (33.3) | 218 (31.5) | 0.5 | 340 (32.1) |
- 7–12 months | 86 (23.4) | 153 (22.1) | 0.6 | 239 (22.6) |
- 13–24 months | 158 (43.3) | 320 (46.3) | 0.3 | 478 (45.2) |
Breastfeed <24 hours |
311 (85) | 550 (79.6) | 0.03 | 861 (81.5) |
Discarded colostrum |
46 (12.6) | 88 (12.7) | 0.3 | 134 (12.7) |
EBF at 5–6 months |
13 (31.5) | 19 (30.6) | 0.6 | 32 (32) |
Currently breastfed |
240 (65.6) | 527 (76.3) | <0.000 | 767 (72.6) |
- 0–6months | 111 (91) | 210 (96.3) | 0.04 | 321 (94.4) |
- 7–12 months | 72 (83.7) | 142 (92.8) | 0.03 | 214 (89.5) |
- 13–24months | 57 (36.3) | 175 (54.7) | 0.000 | 232 (48.6) |
Current use of BMS |
132 (36.1) | 137 (19.8) | <0.001 | 269 (25.4) |
- 0–6months | 31 (23.5) | 34 (24.8) | 0.02 | 65 (24.2) |
- 7–12 months | 38 (28.8) | 43 (31.4) | 0.01 | 81 (30.1) |
- 13–24months | 63 (47.7) | 60 (43.8) | 0.000 | 123 (45.7) |
*mean (95% confidence interval);
**of 100 children aged 5–6 months 37 urban and 63 rural infants;
The following questions were asked: How many hours after the baby is born, did you start breastfeeding? Did you give the colostrum to your baby?
Do you still breastfeed your child?
Yesterday, what food did you give your child?
Of 340 children who were less than 6 months during the survey 94.4% were currently breastfed: 15.9% received BMS as a supplement and 3.2% as a substitute.
Among the older 717 children (7 to 24 months) 14.2% were currently receiving BMS as a supplement and 14.2% as a substitute. Details of IBMS given before the age of 6 months are shown in
Urban n = 366 (34.6%) | Rural n = 691 (65.4%) |
|
Total n = 1057 | Knows at least one BMS |
|
Ever used one BMS before 6 months | 92 (25.1) | 115 (16.6) | 0.000 | 207 (19.6) | |
Age of starting at least one BMS (months) |
5.8 (4.3–5.9) | 4.53 (3.9–5.2) | 0.1 | 4.8 (4.3–5.3) | |
Advance ™ | 5 (1.4) | 11 (1.6) | 0.00 | 16 (1.5) | 244 (23.1) |
Age of starting (months) | 6.77 (4–9.7) | 5.46 (2.2–8.7) | 0.5 | 6 (3.9–8.1) | |
Cereals | 42 (11.5) | 59 (8.5) | 0.1 | 101 (9.6) | 294 (27.8) |
Age of starting (months) | 4.26 (3.6–4.9) | 3.83 (3.4–4.3) | 0.3 | 4.01 (3.6–4.4) | |
Formula | 55 (15.0) | 32 (4.6) | 0.00 | 87 (8.2) | 340 (32.2) |
Age of starting (months) | 2.54 (1.7–3.3) | 2.39 (1.8–3.0) | 0.8 | 2.13 (1.8–2.5) | |
Coffee Creamer | 20 (5.4) | 26 (3.7) | 0.2 | 46 (4.3) | 620 (58.7) |
Age of starting (months) | 2 (1.3–2.6) | 2 (1.5–2.4) | 1. | 2.0 | |
Condensed Milk | 6 (1.6) | 15 (2.2) | 0.7 | 21 (2) | 541 (51.2) |
Age of starting (months) | 4.12 (0.2–8.0) | 5.41 (2.4–8.4) | 0.59 | 2.64 (1.8–3.4) | |
Sterilized Milk | - | 1 (0.1) | - | 1 (0.1) | 236 (22.3) |
Powder Milk | 0 | 1 (0.1) | 1 (0.1) | 142 (13.4) |
*Mean age and 95% confidence interval,
knows at least one BMS in the category.
The following questions were asked: Did you give this product to your baby? If yes, How old was your child when you started giving this product to her/him (month).
BMS were more often recognized in urban areas: 77.5% of the mothers recognized at least one of the BMS: 94.8% vs. 68.3% (p<0.000) in urban and rural areas, respectively. BMS were usually considered as milk by the majority of mothers: 93.9% versus 92.6%, p = 0.4; in urban and rural areas, respectively. Among the non-dairy canned coffee creamer this rate reached 98% for Bear brand™ and 93% for non-Bear brand™. 29.6% of the mothers considered coffee creamer a good product for their babies. Among tetrapaks, Cerelac™ was usually well recognised as a cereal by 52% and had the lowest rate of being mistaken for milk (45%). Formulas and non-Bear brand™ canned BMS were infrequently mistaken for cereal by 2 to 7% of respondents. Characteristics of the five most commonly used products are shown in
Total | Cost |
Duration of use£ | Cost per day |
|
n = 207 (%) | ||||
Cerelac™ | 101 (48.8) | 3.2 | 19 | 0.2 |
Lactogen™ Formula | 75 (36.2) | 7.1 | 12.4 | 0.6 |
Bear brand™ coffee creamer | 30 (14.5) | 0.8 | 7 | 0.1 |
Advance™ |
22 (10.6) | 7 | 6.9 | 1 |
Dumex™ Formula | 14 (6.8) | 10.2 | 11.1 | 0.9 |
*One US$ = 8,000 kip. Mean prices reported by mothers, £ How long does one can or box last or box.
**Main component: Skimmed milk powder (36,5%), full cream milk powder (21,9%,) vegetable fat mix (12,6%), sucrose 7,7%, Maltodextrin 6,7%, honey 5,5%, lactose 3,2%, oligo-fructose (2,6%), butter oil (1,3%), vitamins and minerals premix (0,9%), soya lecithin (0,3%), fish oil (0,1%).
One formula and one non-formula product (Lactogen™ and Cerelac™) accounted for 85% of the products used before 6 months of age (
Commercials on Thai TV (26%) and shopkeepers were the main source of information on BMS (
Urban | Rural | Total | ||
n = 366 (%) | n = 691 (%) |
|
n = 1057 (%) | |
- Heard from |
180(49.2) | 108(15.6) | 0.000 | 288(27.2) |
- TV Lao | 10 (5,5) | 10(9,2) | 0.2 | 20(6,9) |
- TV Thai | 175 (97,2) | 99(91,6) | 0.001 | 274 (95,1) |
- Shop keepers | 18(4.9) | 88(12.7) | 0.000 | 106 (10) |
- Friends | 51(13.9) | 53(7.7) | 0.001 | 104(9.9) |
- Health staff | 13(3.5) | 17(2.4) | 30(2.8) | |
- Posters | 10(2.7) | 5(0.7) | 0.009 | 15(1.4) |
Trust at least in one source |
346 (94.5) | 608 (88) | 0.001 | 954 (90.2) |
- Health Staff | 280 (76.5) | 469 (67.8) | 0.003 | 749 (70.8) |
- Older people | 23 (6.2) | 72 (10.4) | 0.02 | 95 (8.9) |
- TV Thai | 29 (7.9) | 22 (3.1) | 0.001 | 51 (4.8) |
- Radio | 8 (2.1) | 30 (4.3) | 0.05 | 38 (3.6) |
- Family members | 11 (3.0) | 17 (2.5) | 0.6 | 28 (2.6) |
- TV Lao | 14 (3.8) | 11 (1.6) | 0.2 | 25 (2.3) |
- Mother | 5 (1.3) | 10 (2.3) | 0.9 | 15 (2.1) |
- Husband | 7 (1.9) | 6 (0.8) | 0.1 | 13 (1.2) |
The following questions were asked: How did you hear about these products? (many answers possible), if the answer was TV: Which channels?
The following question was asked: Which of the above mentioned sources of information do you trust the most for your family?
Mothers used BMS because they believed the products were a good nutritive complement to breast milk (
Reasons |
Urban | Rural | Mothers | |
n = 89 | n = 114 |
|
n = 203 |
|
Advised by relatives and family | 21 (23.6) | 23 (20.1) | 0.5 | 44 (21.6) |
Safe for baby | 15 (16.8) | 22 (19.3) | 0.6 | 37 (18.2) |
Nutritional value |
20 (22.4) | 17 (14.8) | 0.1 | 37 (17.4) |
Complementary feeding | 17(19.1) | 31 (27.6) | 0.1 | 48 (23.8) |
Work (too busy to breastfeed) | 11 (57.8) | 8 (7.1) | 0.2 | 19 (9.3) |
Cannot breastfeed | 4 (4.4) | 10 (8.7) | 0.1 | 14 (6.9) |
Health staff advice | 6 (6.7) | 8 (7.0) | 0.9 | 14 (6.9) |
Easy to use | 3 (3.3) | 6 (5.2) | 0.7 | 9 (4.4) |
Infant loves it | 4 (4.4) | 4 (3.5) | 0.7 | 8 (3.9) |
Weaning | 3 (3.3) | 2 (1.7) | 0.4 | 5 (2.4) |
Advertising | 3 (3.3) | 2 (1.7) | 0.4 | 5 (2.4) |
Cheap | 2 (2.25) | 0 | 0.1 | 2 (1) |
The following question was asked: Why do you feed your baby this product?
*Of 207 users before 6 months, 203 users ‘responses available.
**Rich with vitamins, similar to rice, good for children.
***1.4% of 1057 mothers reported that they could not breastfeed.
Mothers with no education, but having a radio were 4.5 and 2 times more likely to consider breast milk better than BMS. Unemployed mothers living in rural areas were less likely to consider BMS better than breast milk (multivariate analysis, data not shown). The multivariate analysis between selected independent variables and BMS used before 6 months is shown in
Ever used one BMS before 6 Months | OR | 95% CI |
|
Lao Loum | 1.8 | 1.2–2.8 | 0.01 |
Buddhist | 1.8 | 1.1–2.9 | 0.01 |
House made of concrete | 1.6 | 1.1–2.5 | 0.02 |
House with latrine | 1.5 | 1–2.2 | 0.07 |
Mother breastfed colostrum | 0.6 | 0.4–1 | 0.05 |
95% Confidence Interval.
Optimal breastfeeding of children under 2 years of age has the potential to help prevent 1.4 million deaths annually in children under 5 in the developing world
This may still impede the objectives of the Millennium Development Goals. This survey provides baseline data on BMS use and suggests some clues on how to improve promotion of breastfeeding in countries similar to Laos.
In this survey we found some differences between values reported in the Laos Reproductive Health Survey (LHRS) and the National Maternal and Child Nutrition Survey (MICS survey) which could probably be explained by the higher proportion of urban mothers, and the restricted access to remote rural areas in this survey (urban: 34.6% versus 28% in MICS and 9.8% in LRHS)
Among children less than 6 months mothers used BMS more often (15.9%) as a supplement than as a substitute (3.2%). However, after 6 months the use of BMS as a substitute increased to a similar rate (14.2%). Mixing BMS with breastfeeding can hamper and reduce the quality and duration of breastfeeding
A quarter of the population were currently feeding their children with at least one BMS and 20% reported starting before 6 months (at least one non-formula: 83%). Of concern is the fact that some BMS were non-dairy products. The use of BMS may have hampered the EBF rate and benefits and shortened the well-established tradition of long durations of breastfeeding
The 2009 survey which only interviewed mothers with children less than 2 years of age (versus 63.6% of mothers in 2007 survey) probably had less recall bias than the 2007 survey exploring the use of coffee creamers. The current survey, which includes more provinces (12 versus 5), more rural (65.4% versus 51%) and more illiterate people (20% versus 10%) is also probably more representative. It shows a decreasing trend in the use of coffee creamer for infants previously described (3.8% in 2009 versus 18% in 2007, p<0.001) which is a real improvement
There seems to be no replacement by other coffee creamer or condensed milk brands in Laos. The other brands are labelled with pictures unrelated to mothers and children (such as tea pots, flowers, cakes etc). This supports our previous statement that the Bear brand™ was highly misleading to the population. We, and others, reported additional obvious violations of the International Code on the Marketing of Breast-milk Substitutes
The Bear brand™ coffee creamer remains popular and the most recognized product by mothers. The licensed trade mark using the misleading Bear brand™ label is still widely available in Laos and Thailand and remains a cause for great concern
Financial reasons (daily food expenses per family: USD 2.00 versus USD 4.20 for rural and urban, respectively) and lower accessibility to BMS in rural areas explain the higher rate of BMS use in urban areas. An important reason is the higher exposure to misleading advertising from Thai TV that we found in urban and rural areas. Mothers repeatedly exposed to advertisements for infant formula expressed interest in buying them
Lao mothers are highly influenced by their relatives in the decision making process for/against breastfeeding. Among relatives, involvement of the child's father can influence breastfeeding choices
Mothers who fed colostrum to their babies (a recent achievement of the past 10 years) tended to use BMS less. Antenatal care was higher than 70%. This, and the high trust in health staff reported in the survey, confirms the role of antenatal care in Laos. More attention should be paid during antenatal care to allow mothers to make an informed choice on breastfeeding. Fathers should be invited to participate in antenatal care and educational programmes, thus encouraging them to play a more supportive role in breastfeeding. This should be encouraged in the community. Hospital staff have a positive influence on breast feeding practices but this intervention has to be reinforced in the community to ensure long term sustainability
The final multivariate analysis suggests that mothers with higher living standards were at higher risk of using BMS. Nearly all of them reported that they believed that BMS was real milk. They considered these products a good nutritive complement to breastfeeding. However, they had different feelings regarding the quality of the products. Cereals and formula which are attractively packaged, and highly priced, were the first choice and canned products the last. Advance™ follow-up formula, displayed in a similar manner to cereals and formula, was among the last choice (
In developing countries substituting breastfeeding, to avoid, for example HIV transmission, is nullified by increases in non-infectious child mortality resulting in no net benefit for HIV-free survival
The poor knowledge of mothers regarding BMS suggests that EBF could improve through nationwide information campaigns. Breastfeeding should be promoted through TV advertising and breastfeeding campaigns. Such intervention resulted in the improvement of breastfeeding practices in the Philippines
Health authorities should focus on urban mothers but persist in maintaining appropriate messages towards the rural population as well, to prevent a decrease of breastfeeding, similar to that observed in the region. Important measures can be taken to enforce the International Code of Marketing of Breastmilk Substitutes, which Laos endorsed at the 1981 World Health Assembly. Legislation requires good enforcement and the support of UNICEF and international organizations to guarantee that child health workers and health professionals are protected from exposure to BMS companies. A programme to support breastfeeding could include the following components: monitoring violations of the Code; increasing advocacy and information of EBF among health staff; families with breastfeeding mothers; the general population; teenagers; and during all reproductive health services. Labelling of BMS should be improved and translated into the local language. The display and sale of non-formula products next to products intended for infant feeding should also be prohibited. It is the responsibility of manufacturers to respect the Code in the neighbouring countries
Inappropriate use of BMS for infants less than 6 months of age represents a threat to the preservation of the high breastfeeding rate in Laos and will hamper any improvement in EBF rates. Action should be taken to decrease the impact of misleading advertising, which influences mothers to switch from traditional breastfeeding to BMS. Enforcement of the International Code of Breastmilk Substitutes will protect and promote breastfeeding. Successful educational tools should be developed to promote, sustain and improve the quality of breastfeeding. Improved breastfeeding practices will save infant lives.
We thank the IFMT students of P10 class (Drs. T Thaoboualy, K Vongphayloth, G T Edosoa, S Inthavilay, V Souvong, V Hansackda, B Chaykaodaxue, V Gnothlysack, Thierry Franchard) and IFMT staff and teachers (among them, Dr. P Naphayvong), Health Frontiers, Service Fraternel d'Entraide (Dr. G Slesak), and all the people who participated in collecting data during the surveys and all families participating in the surveys. We are particularly grateful for Dr. L Srour kind support, helpful comments and collaboration, and Pr. Y Buisson for comments. We thank Percy Aaron and L Srour for editing and revising the drafts. We thank the Lao national and regional health authorities for their support.