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Effect of Sequencing of Complementary Feeding in Relation to Breast-Feeding on Total Intake in Infants

Shah, Dheeraj; Singh, Meenakshi; Gupta, Piyush; Faridi, M.M.A.

Journal of Pediatric Gastroenterology and Nutrition: March 2014 - Volume 58 - Issue 3 - p 339–343
doi: 10.1097/MPG.0000000000000219
Original Articles: Hepatology and Nutrition

Objective: The aim of the present study was to evaluate whether the order of complementary feeding in relation to breast-feeding affects breast milk, semisolid, or total energy intake in infants.

Methods: The present study was designed as a randomized crossover trial. The study was conducted in a tertiary care hospital. The study participants were 25 healthy infants between the ages of 7 and 11 months who were exclusively breast-fed for at least 6 months and were now receiving complementary foods for at least 1 month in addition to breast-feeding. Infants were randomized to follow a sequence of either complementary feeding before breast-feeding (sequence A) or complementary feeding after breast-feeding (sequence B) for the first day (24 hours) of the study period using simple randomization. For the next day, the sequence was reversed for each child. All babies received 3 actively fed complementary food meals per day (morning, afternoon, and evening). A semisolid study diet was prepared in the hospital by cooking rice and pulse with oil using a standard method, ensuring the energy density of at least 0.6 kcal/g. The infants were allowed ad libitum breast-feeding during the observation period. Semisolid intake was directly measured and breast milk intake was quantified by test weighing method. Energy intake from complementary foods was calculated from the product of energy density of the diet served on that day and the total amount consumed. The total energy intake and energy intake from breast milk and complementary foods between the 2 sequences were compared.

Results: The mean (standard deviation) energy intake from breast milk during 12 hours of daytime by following sequence A (complementary feeding before breast-feeding) was 132.0 (67.4) kcal in comparison with 135.9 (56.2) kcal in sequence B, which was not statistically different (P = 0.83). The mean (standard deviation) energy consumed from semisolids in sequences A and B was also comparable (88.6 [75.5] kcal vs 85.5 [89.7] kcal; P = 0.58). The total energy intake during daytime in sequence A was 220.6 (96.2) kcal in comparison with 221.5 (94.0) kcal in sequence B, which was also comparable (P = 0.97). The results related to energy intake through breast milk and total energy intake were not different when insensible losses during feeding were adjusted in both groups.

Conclusions: Altering the sequence of complementary feeding in relation to breast-feeding does not affect total energy intake.

Division of Pediatric Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, University College of Medical Sciences (University of Delhi) and Guru Tegh Bahadur Hospital, Dilshad Garden, Delhi, India.

Address correspondence and reprint requests to Dr Dheeraj Shah, Department of Pediatrics, UCMS & GTB Hospital, Dilshad Garden, Delhi-110095, India (e-mail:

Received 15 October, 2013

Accepted 15 October, 2013

The authors report no conflicts of interest.

See “Complementary Feeding: Keeping the Message Simple” by Briend and Dewey on page 275.

Appropriate feeding practices are of fundamental importance for the survival, growth, development, health, and nutrition of infants and children (1,2). Complementary feeding is recommended to be started at 6 months of age with continued breast-feeding to fill the nutrient gap created by the increase in energy requirement and with a reduction in milk output at this age (2,3). Infants from developing countries often do not achieve the recommended energy and nutrient intake, and thus are at risk of malnutrition and growth failure during this critical period of complementary feeding. Innovative methods are, thus, required to achieve an increase in the nutrient intake of a breast-fed child during this period of complementary feeding.

Breast milk, being rich in energy, high-quality proteins, and other nutrients provides a major portion of nutritional needs even in a complementary fed child. Any recommended method of complementary feeding, thus, should not interfere with intake of high-quality breast milk. All foods and liquids, including water, however, are likely to interfere with the amount of breast milk ingested by young infants (3–6). It is, thus, critical to achieve a positive balance between the amount of additional energy supplied from complementary feeding and the amount of energy reduced because of lower breast milk intake. It is important to evaluate whether the sequence of breast-feeding in relation to complementary feeding, that is, breast-feeding given shortly before or after a complementary food meal, affects the total energy intake in an infant (2,7). Although some programs recommend breast-feeding before offering other foods (2,8), there is no evidence-based recommendation available about the sequence to be followed, and it is not known whether a particular order can influence the total energy intake. The present study was planned to evaluate the effect of sequencing of breast-feeding in relation to complementary feeding on the energy intake from breast milk and semisolid foods in infants.

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The present study was designed as a randomized crossover trial conducted in the pediatric ward of a tertiary care hospital in India during a period of 9 months (April 2008–December 2008). The study protocol was approved by the institutional review board, including ethical clearance. A written informed consent was obtained from the parents/caregivers of all of the included children.

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Inclusion Criteria

Healthy infants between 7 and 11 months of age having normal weight (weight-for-age ≥−2 standard deviations [SDs] of the World Health Organization standard) formed the subjects for this trial. Infants who received exclusive breast-feeding until at least 6 months of age and were receiving complementary foods in addition to breast-feeding for at least 1 month were eligible for inclusion in the present study. These children were recruited from among the normal siblings of older hospitalized children, healthy volunteers (parents), or those recovering from minor illnesses such as upper respiratory tract infection, pyoderma, and noninfective seizures.

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Exclusion Criteria

Infants who were febrile (temperature >38°C) or suffering from conditions that per se interfere with feeding (oral ulcers, oral candidiasis, cerebral palsy, cleft palate) were excluded. Infants who were suffering from any chronic ailment (eg, congenital heart disease, chronic lung disease, hepatic or renal disorders, central nervous system malformations) were also excluded.

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The infants were randomized (simple randomization using random number table) to follow a sequence of either complementary feeding before breast-feeding (sequence A) or complementary feeding after breast-feeding (sequence B) during the first day (24 hours) of the study period. Allocation concealment was done by concealing the code in opaque sealed envelopes. For the next day, the sequence was reversed for each child.

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Sequence A

Complementary feeding was given to the child when the mother believed that the child was hungry. When the child was no longer interested in semisolid food, the baby was breast-fed until satisfied. In case the child was not interested, the mother tried again after every 10 minutes up to 30 minutes.

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Sequence B

The mother fed the complementary food immediately after the process of breast-feeding was over during these 3 meals. In case the child was not interested, she tried again after every 10 minutes up to 30 minutes.

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The recruited subjects were kept with their mother in the hospital ward for at least 48 hours. Baseline weight (using a digital weighing scale with a sensitivity of 5 g) and length, mid-upper arm circumference, and head circumference (using measuring tape sensitive to 1 mm) were recorded for all of the infants, and the weight-for-age, height-for-age, and weight-for-height z scores were calculated in relation to World Health Organization standards (9). The procedure was explained to the mother and she was instructed to give ad libitum breast-feedings throughout the day. Three complementary food meals per day (morning, afternoon, and evening) were provided, and the breast-feeding was sequenced before or after these meals based on the randomization. Nothing else was allowed to be given to the child during the study period except sips of water. Detailed medical, birth, immunization, and developmental histories were taken. A feeding history was taken, including time of initiation, type of food, and consumption of fruits, green leafy vegetables, eggs, and nonvegetarian food. Sequence of feeding followed at home was inquired about using the 24-hour recall method.

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Intervention and Measurements

All of the babies received 3 complementary food meals per day (morning, afternoon, and evening). The semisolid study diet was prepared in the kitchen by cooking rice and pulse with oil in the ratio of 2:2:1 with water and salt in the conventional manner to simulate the diet given at home. The diet had an energy density of at least 0.6 kcal/g as per recommendations for this age group (2). The energy density of the diets was calculated using the calorific content of raw ingredients (rice, pulse, and oil) available for Indian foods (10) and the cooked weight of the prepared diet. Milled rice, green gram, and sunflower oil were used with energy contents of 345 kcal/100 g, 348 kcal/100 g, and 90 kcal/10 mL, respectively (10). Mothers were encouraged to actively feed the infants with a cup and spoon until they refused to accept the feed on 3 consecutive offers. Infants were allowed ad libitum breast-feeding during the observation period. No other food or fluid besides water was allowed during the study period.

Semisolid intake was quantified by weighing the container both pre- and postfeed, taking care to account for spillage. Energy intake from complementary foods was calculated from the product of energy density of the diet served on that day and the total amount consumed. Breast milk intake was quantified for 12 hours during the daytime by the test weighing method. Infants were weighed wearing preweighted diapers to account for losses in the form of urine and stool and the duration of feeding was noted. For each infant, the insensible water loss (ISWL) was estimated by weighing the infants (with preweighted diapers) in the morning, afternoon, and evening at 1-hour intervals. The amount of breast milk consumed by the child was measured by weighing the child with preweighed diapers before and after the breast-feeding. The amount calculated could be underestimated, because the child would lose some weight because of sweating (ISWL) (11). ISWL was calculated by noting the duration of breast-feeding during the observation period. The weight loss as a result of ISWL in 1 hour was noted at 3 different times of the day, ensuring no feeding during that hour. The average of the weight loss per hour was calculated. Using the average ISWL in 1 hour for the child and duration of breast-feeding, ISWL during breast-feeding was calculated. Therefore, to account for the ISWL, corrected breast milk and corrected total energy consumed were calculated by adding the ISWL to the apparent breast milk intake and apparent total energy intake.

The energy intake from breast milk was estimated assuming an energy density of 0.67 kcal/g (2,12). The semisolid intake for each infant was calculated for all 3 feeds. The breast milk intake was recorded during the 12 hours of daytime, including feeds given along with complementary feeding.

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Sample Size

Using SD data from previous studies (13,14) on energy density and frequency, a sample size of 23 infants enrolled in a crossover manner was determined to be adequate to detect a difference of 5 kcal · kg−1 · day−1 in total energy intake between the 2 methods (sequence A and sequence B) with 95% confidence and a power of 90%.

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Statistical Analysis

The data were entered into a Microsoft Excel worksheet. Data were analyzed using SPSS version 12.0 software (SPSS Inc, Chicago, IL). The mean values of energy (kilocalorie), breast milk (milliliter) and semisolid (gram) intake during 12 hours of daytime were compared between sequence A and sequence B using the paired Student t test.

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Twenty-five children were randomized out of 41 children approached for the study purpose (Fig. 1). Twelve children were randomized to group A and 13 to group B for the first day of the study. Infants in group A received complementary feeding followed by breast-feeding (sequence A) on day 1 and those in group B received breast-feeding followed by complementary feeding (sequence B) on day 1 (Fig. 1). The sequence was reversed in both groups on day 2. There were a total of 25 subjects in both sequences for all outcomes because of the crossover nature of the trial.



The mean (SD) age of the included children was 9.0 (1.3) months. About two-thirds (68%) of the included subjects were boys. Seventeen (68%) subjects were healthy volunteers, and 7 were recovering from minor illnesses. One child was the sibling of another admitted child. The mean (SD) age of initiation of complementary feeding was 6.2 (0.6) months. Table 1 compares the baseline characteristics between 2 groups. Age at enrollment, anthropometry, and maternal education status were comparable between the groups. Energy density of complementary food was comparable during sequence A or sequence B (Table 2).





Table 2 compares the mean (SD) breast milk consumed in 12 hours by following sequence A or sequence B. Breast-milk intakes and energy intakes from breast milk (apparent and corrected) were comparable in infants following either sequence. Energy consumed from complementary feeding and the total energy intake were also comparable in infants following sequence A or sequence B. Differences in energy intakes were not significant even after correcting for ISWLs.

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The order in which complementary feeding and breast-feeding should be given has been identified to be an important research priority (2,7). In this crossover trial of infants who were continued to be breast-fed while on complementary feeding, we could not demonstrate any effect of sequence of complementary feeding in relation to breast-feeding (complementary feeding before or after breast-feeding) on either total energy intake or energy intakes from breast-milk or complementary foods.

The crossover design of the trial potentially eliminated the biases owing to individual appetite, feeding behavior, and preferences of the children. Randomization for selecting the sequence on the first day owing to the different environment of the hospital. The possible limitation of the study was the recording of breast milk intake for a period of only 12 hours during the daytime, which resulted in a general underestimation of total energy intake because infants consume a significant amount of breast milk at night (15,16). The comparison of 2 sequences is still likely to be valid because it is unlikely that the amount from breast milk will vary in between the sequence because no complementary feeds were given in the nighttime as per usual practice in the country. Second, the methods of testing used by us for detecting breast milk intake and ISWLs were relatively crude. The reference method, using deuterium oxide dilution, could not be used in the present study because this requires approximately 2 weeks for a correct measure, which would be unsuitable for the study objectives. Another potential limitation is the change in one sequence to another in only 1 day; a longer period could have resulted in more robust estimates.

Nonbreast milk food and fluids are known to decrease the breast milk energy consumption in a breast-fed infant (3–6). Estimates indicate that each kilocalorie from a nonbreast milk source displaces about 0.6 kcal of breast milk between 16 and 26 weeks of life; estimates for infants >6 months of age are not available (7). The results from our study suggest that the displacement of breast milk energy is not much different whether complementary foods are given before or after breast-feeding. The infant's appetite and feeding behavior seems to regulate his or her energy intake within a narrow range and any change in the characteristic of diet or the method of feeding does not greatly influence it beyond a certain limit. Earlier studies on the changes made in the energy density of the complementary foods (13), frequency of feeding (14), and sequence (17) also showed that there is a close relation between the energy consumed from breast milk and complementary foods in a breast-fed infant. Any changes made in the one affects the other, thus balancing the total energy intake.

We conclude that there is no difference in total energy intake, breast milk intake, and complementary feeding intake, irrespective of whether complementary feeds are given before or after breast-feeding, and thus total energy intake is unlikely to be increased by altering the sequence of breast-feeding in relation to complementary feeding. The results of our study are applicable to apparently healthy infants consuming a vegetarian rice pulse gruel diet, and may not be valid for other settings, including undernourished children. Community-based studies in different settings using a longer duration for each sequence are needed to confirm our findings.

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Protocol (Treatment) for Huo Luan (Gastroenteritis) from the Ishimpo (982 CE) or Fecal Microbial Transplantation: “What Is Past, Is Prologue…”

Bing Yuen Lun stated: The stomach and intestine of a child is young and weak. If the child catches cold when undressed he will be unable to digest the milk resulting in vomiting and diarrhea. Or if the wet nurse catches cold or eats cold or raw food she will allow cold qi* to enter the milk. In this case, feeding the child will also cause Huo Luan.

Qian Jin Fang protocol for Huo Luan in children: Feed the child with 1 ge of cow saliva.

Another protocol: Feed the child with warm juice of cow dung.

Another protocol: Grind the cow dung and feed 3 dao gui (cinnamon) with milk, three times daily.

Tamba, Ishimpo, Protocol 103


Life force or energy.

The Ishimpo is the oldest extant Japanese medical text. It was compiled by Yasuyori Tamba (911–995 CE) in 982 and presented to the Emperor Enyu in 984. Tamba compiled and recorded verbatim information from all of the available Chinese medical and pharmacologic texts of the Sui (581–618 CE) and Tang (618–907 CE) dynasties—some 204 texts—resulting in the thirty scrolls that comprise the Ishimpo. Almost all of these primary sources have been lost, making the Ishimpo the most valuable source of classical Chinese medicine. (Of the 204 works cited in the Ishimpo, 180, or 88%, are now lost.)

Protocol 103, from the pediatric scroll number 25, is a classic example of Dreckapoteke (scatological pharmacy), which incorporates the medicinal compounding of dung, urine, menstrual flow, and other biological byproducts.

—Contributed by Angel R. Colón, MD

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breast-feeding; feeding behavior; infant nutritional physiological phenomena

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