Semin Neonatol 2002; 7: 231239 doi:10.1053/siny.2002.0110, available online at http://www.idealibrary.

com on

Breast-feeding multiples
O. Flidel-Rimon and E. S. Shinwell

Department of Neonatology, Kaplan Medical Center, Rehovot, Hebrew University, Jerusalem, Israel

Key words: multiple pregnancy, breast-feeding, lactation, twins, triplets

Human breast milk is the best nutrition for human infants. Its advantages over the milk of other species, such as cows, include both a reduced risk for infections, allergies and chronic diseases, together with the full nutritional requirements for growth and development. Breast-feeding is as important for multiples as for singletons. Despite the advantages, multiples receive less breast-feeding than singletons. Common reasons for not breast-feeding multiples include the fear of not fullling the infants needs and the difficulty of coping with the demands on the mothers time. In addition, many multiples are delivered prematurely and by Caesarean section. Maternal pain and discomfort together with anxiety over the infants condition are not conducive to successful breast-feeding. During lactation, the mother needs to add calories to her daily diet. It has been recommended to add approximately 500600 kcal/day for each infant. Thus, between eating, nursing and sleeping, life is very busy for the mother of multiples. However, there is evidence that, with appropriate nutrition, one mother can nourish more than one infant. Also, simultaneous breast-feeding can save much time. Combined efforts of parents, close family, friends and the medical team can help to make either full or partial breast-feeding of multiples possible. However, when breast-feeding is not possible, health care workers need to carefully avoid judgmental approaches that may induce feelings of guilt.  2002 Elsevier Science Ltd. All rights reserved.

Introduction
Human breast milk is specic for the needs of the human infant. Its unique composition provides the ideal nutrients for growth and development during the rst year of life. Many studies have combined to demonstrate the superiority of human milk over that of other species. Breast-fed infants demonstrate better neurodevelopment outcome [13]. Leukocytes, specic antibodies and other antimicrobial factors protect the breast-fed infant against common infections such as gastroenteritis, upper respiratory tract infection, sepsis, otitis media, urinary tract infection and meningitis [48]. Epidemiological studies have revealed a reduced incidence of chronic childhood diseases such as lymphoma, insulin dependent diabetes mellitus,
Correspondence to: Eric S. Shinwell, MD, Department of Neonatology, Kaplan Medical Center, P.O. Box 1, Rehovot, Israel. Tel.: (972) 89441218; Fax: (972) 89441768; E-mail: erics@clalit.org.il

Crohns disease, obesity and allergies [911]. There are many psychological and cognitive benets for the breast-fed infant [1,2,12]. Thus, it is well established that breast milk is the best food for babies and that breast-feeding is benecial to maternal health [13]. Breast-feeding multiples is, in principle, the same as for singletons, but there are many potential difficulties and a great deal of support is needed. Multiple pregnancies are often associated with Caesarean section delivery, prematurity and low or very low birth weight infants. Premature infants are prone to develop postnatal complications including: recurrent episodes of sepsis (1630% of the preterm born less than 1500 g or VLBW), necrotizing enterocolitis (112% of the VLBW infants) and retinopathy of prematurity (2050% of VLBW) [14,15]. In view of the advantages of breast milk in preventing or ameliorating these complications, these infants may benet the most from breast milk
2002 Elsevier Science Ltd. All rights reserved.

10842756/02/$-see front matter

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and yet it is more difficult to achieve breastfeeding for them [16]. Likewise, mothers of multiples are most in need of a good start to breast-feeding and yet they are the mothers least likely to achieve it. Parents of twins and high-order multiples, in particular, need support in four major areas: organization, feeding, individualization and stress management [17]. For example, Robarge compared sources of stress in families rearing twins as compared to singletons. The simple matter of feeding infants was found to be signicantly more stressful for mothers of twins [18]. Medical care providers often nd difficulties in providing advice and support to these families. In this review, we will try to answer some of the main issues regarding breast-feeding multiples.

How well do mothers succeed in breast-feeding multiples and what are the common reasons for stopping?
As mothers of multiples are a unique group, who are often not expected to breast-feed, few studies have been reported on this question. One study that was reported in 1975 by Addy revealed that, in a selected group of members from a Mothers of Twins club in southern California, only 24% (41/ 173) were breast-fed from birth [19]. Of these, 37% (15/41) breast-fed for less than a month and only 20% (8/41) continued for 46 months. Reasons for introduction of supplements were inadequate breast milk in 28%, failure of the twins to thrive in 13%, local illness such as breast engorgement, retracted nipples or abscess in 15%, maternal illness in 7% and, only in 2% of the cases was an illness of the twins reported the cause for stopping breastfeeding. The reasons for not starting were that the mother did not want to breast-feed in 36%, maternal or infant illness in 8 and 9% respectively, physician advice against in 9%, not enough milk in 8% and not enough time in 11% Although the rates above seem very low, there is conicting evidence as to the comparison of breast-feeding rates between singletons and multiples. Recent data from a national mothers survey in 1990 found no signicant difference in initiation of breast-feeding between mothers of twins (48%) and singletons (51%). Likewise, at

6 months, 13% of twins and 18% of singletons were still breast-feeding [20,21]. In addition, Kerkhoff quoted Maureen Boyle of Mothers of Super Twins (MOST) that, during 1997, the rate of initiating breast-feeding was close to 70% for 800 new mothers. This, however, may well represent the rates that can be achieved in a highly motivated selected group. No follow up data concerning breast-feeding after discharge from the hospital was reported. However, as many multiples are born prematurely, assessments of the success of breast-feeding multiples must include this high-risk group. Liang and co-workers compared singleton and twin preterm infants of 2936 weeks of gestation [22]. The multiples tended to start as partial and progress later to exclusive breast-feeding. Overall, 93% of singletons and 89% of twins were on breastfeeding at discharge from the hospital. Also, there was a similar rate of decline in breast-feeding rates among singletons and twins to 68% at the age of 812 weeks and 49% at the age of 1216 weeks after birth. By comparison, Czeszynska and co-workers studied premature multiples of mean gestational age of 35.6 weeks and found that, despite an intensive promotion programme, it was rare that multiples were discharged on exclusive breast-feeding [23]. Most of the families were using a combination of breast milk with infant formula. Factors that were associated with delaying early breast-feeding included respiratory distress in 22%, infections in 28%, Caesarean section in 62% and maternal medications in 14%. Most of the infants start to breast-feed only 34 days after the delivery. Rozas studied the factors that inuence the success of breast-feeding in mothers of twins [24]. The main reason given for starting breast-feeding was the knowledge it was better food for the baby. Women with prior counselling started breastfeeding in greater numbers than those not counselled. Factors that did not inuence breast-feeding in this study were maternal age, birth type, birth weight, maternal education, work and domestic situation and admission to the newborn unit. However, this was a small sample of relatively mature sets of twins in Spain and may not be representative of all multiples. These data demonstrate the need for special efforts in promoting breast-feeding among mothers of multiples. A particular source of anxiety to be addressed is the nutritional adequacy of breast milk for multiples.

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To what extent can breast milk be considered nutritionally satisfactory for multiples?
A consistent nding in the media or in Internet sites that deal with multiples is the concern of mothers as to whether there is enough milk for more than one baby. As mentioned above, this results in a greater tendency to introduce articial feeding to twins for fear that breast milk alone may be inadequate. Thus, can breast-feeding be considered satisfactory in the feeding of multiples, particularly in the early months of life? An historical answer may be wet nurses, who could be viewed as having been the historical intermediate alternative between maternal breast milk and articial formula. In foundling homes in France during the 17th century, each wet nurse fed 36 infants, who were often of differing ages and with different daily requirements [25,26]. Another source of evidence that women can provide enough milk for more than one infant comes from milk banks. These were opened rst in Vienna in 1900 and later at the Massachusetts Infant Asylum [27]. The milk provided to these banks was surplus from nursing mothers and was made available to other infants whose mothers were unable to provide adequate milk. Thus, clearly, certain women are capable of expressing adequate volumes of milk for more than one infant. Emmett and Rogers showed that, over the course of lactation, the volume of human milk produced is directly related to the weight of the infant [28]. Thus, if volume is related to demand, two babies of 3 kg each may be equivalent one of 6 kg. Saint and co-workers studied the volume and composition of milk produced by mothers of singletons, twins and triplets [29]. The milk yield of mothers was determined by measuring the decrease in the mothers weight, by beam balance, at each feed over a period of 24 hours. Mothers of twins consistently produced twice the volume of milk as mothers of singletons. Mothers of triplets were capable of producing up a remarkable volume of more than 3 litres/day when the infants were aged 2.5 months. The concentrations of lactose, protein and mixed fat in the milk were variable but adequate in all groups of mothers. Thus, both the volume and content of breast milk can be adequate to feed multiples and therefore, mothers may be advised that the more

she nurses, the more adequate her milk supply will be.

What are the nutritional requirements during pregnancy and lactation?

1. Singleton pregnancy The mothers body prepares itself during pregnancy for the process of lactation by developing the breast to produce milk and also by storing energy. An important physiological change in the mothers body during pregnancy is the deposition of fat. During normal full-term pregnancy there is an addition of approximately 4 kg of fat deposit [30,41]. Protein metabolism is also changed during pregnancy and it is suggested that there is also a maternal gain of fat-free tissue [31]. Women who breast-feed their infants probably lose most of the additional fat that was laid down during pregnancy unless they consume a very high intake diet. The Subcommittee on Nutrition during Lactation of the Institute of Medicine recommends that the daily nutritional supplement during a singleton pregnancy needs to include 300 kcal, 20 g of protein and 20% excess in all recommended daily allowances for vitamins and minerals. Specic exceptions are a double dose for folic acid and a 33% increase in calcium, phosphorous and magnesium [32,33]. Milk quantity, protein content and calcium content are relatively independent of the maternal nutritional status and diet. Amino acids, certain fatty acids and water-soluble vitamins content vary with intake. 2. Multiple pregnancy It is very important to prepare the mother during a multiple pregnancy for the task of feeding the coming newborns by giving the appropriate information and by closely follow up after weight gain. Lactation requires caloric energy. The energy comes mainly from two sources: maternal storage of fat and protein during pregnancy and ongoing dietary intake during lactation [34]. Nutritional factors inuence the course and outcome of multifetal pregnancy. The linear

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relationship between weight gain during pregnancy and birth weight is similar in both twin and singleton pregnancy [35]. Consequently, as weight gain during pregnancy is a reliable and simple measure, many studies use it to evaluate nutritional status and pregnancy outcome. It has been shown that maternal weight gain during pregnancy of 2024 kg is associated with birth weights of 2500 3000 g in twins [36,37]. Conversely, low weight gain, or even weight loss during twin pregnancies is associated with preterm delivery [38]. Brown and Carlson made a theoretical calculation of the caloric requirements for adequate weight gain during pregnancy [39]. In order to achieve a weight gain of 5 kg above that of singletons, mothers of twins need an extra intake of 150 kcal/day. Thus, suggested target weight gains for multiple pregnancies may be as follows: a) Twin pregnancy: the recommended overall weight gain is 1620 kg (3541 lb), with an average of 0.65 kg (1.5 lb)/week during second and third trimesters of the pregnancy. The total weight gain in the rst trimester should be of the order of 1.82.7 kg (46 lb). b) Triplet pregnancy: Data from a study of 4 triplet pregnancies suggest a weight gain of 2223 kg (50 lb) with a steady increment of approximately 0.65 kg (1.5 lb)/week throughout pregnancy [40]. c) In a case study of a quadruplet pregnancy, a 3000-kcal/day diet, with 100 g of protein was associated with positive infant outcomes [40]. In addition, women in multifetal pregnancies require counselling regarding nutritional supplements. The National Academy of Sciences (USA) recommends supplements including 30 mg of iron, together with low to moderate doses of zinc, copper, calcium, vitamin B6, folate, vitamin C and vitamin D after 12 weeks of multifetal pregnancy [42]. Increased needs for other nutrients may best be met by increased consumption of nutrient dense food. Adherence to these recommendations should ensure the energy stores needed later for breast-feeding.

3. Lactation singletons and multiples It is possible to calculate the energy required for milk production by assessing three factors the average quantity of milk produced, the caloric content of the milk and the efficiency of milk

production [34,43]. The total amount of breast milk produced can be up to 1.2 l/day during the rst month after delivery and 2 l/day in the second month. The average energy content is 6775 kcal/ 100 ml and the efficiency of production is 8090%. Thus, at the end of the second month of nursing twins, the mother will require a supplement of approximately 1500 kcal/day. Current recommendations for caloric supplementation during breast-feeding are 500600 calories per baby per day [48]. A mother nursing multiples will thus use a combination of reserves stored during pregnancy and increased intake during lactation. The diet should be well balanced (protein 20% of total calories, carbohydrates 40% and fat 40%), should include vitamin supplements and many mothers may benet from the help of an expert, such as a nurse, a lactation counsellor, a physician or a dietitian. Adverse maternal conditions such as dehydration or malnutrition may inuence this process. For example, the volume of the milk may fall as a result of severe dehydration (of 10% of the total blood volume). Additionally, Smith studied the effect of maternal malnutrition on newborn infants in Holland during the Second World War. Malnourished mothers produced a smaller volume of milk but the duration of lactation was unchanged [45]. Studies of malnourished mothers in the third world have likewise shown only a mild decrease in quantity without any change in quality [46,47]. Extreme vegetarian or vegan diets may result in inadequate intake of specic nutrients which may inuence the content of human milk [49,50]. Stress is also believed to interfere with lactation performance via a number of potential mechanisms. These include inhibition of oxytocin release, increased adrenocorticotrophin-releasing hormone and activation of the peripheral sympathetic nervous system. However, psychological studies have failed to show a consistent correlation between measures of stress and lactation performance. Despite this, stress-reducing interventions, such as skin-to-skin contact between the mother and the infant and relaxation therapy have been shown to improve lactation performance and prolong breast-feeding [51,52] Breast-feeding multiples, in particular, with its attendant nutritional demands and lack of sleep, is a potentially stressful situation which may inuence lactation performance. Mothers of twins may be aware of what they should be eating but may

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Figure 1. Mother feeding twins in the double football position.

be unable to live up to such stringent demands. Thus, the importance of time management during lactation raises the issue of the different modes of breast-feeding.

Sides Another issue is whether to alternate breasts between the babies or to assign each baby to the one breast? It is preferable to alternate breasts when breast-feeding twins. This assures that each breast receives balanced stimulation from the different babies and assures that the milk yield for each baby will be the same regardless asymmetrical development or previous surgery in one breast. Positions for simultaneous breast-feeding There are three commonly used positions for simultaneous breast-feeding [20,54]. 1. Double football As shown in Figure 1, an infants head is supported in each of the mothers hands (or on a pillow) with an infants body lying under each of mothers arms. Many mothers use this position initially until they gather more experience. 2. Double cradle In this position each infant is held like a singleton, in the cradle position. The two infants cross on the mothers abdomen (see Fig. 2). This position is often used when the mother is more experienced and the infants have better head control.

Management of breast-feeding time, sides and positions

Time Twins may be breast-fed in any one of three modes: simultaneously, separately on an individual demand schedule or separately on a modied demand schedule where one infant is fed on demand and then the other immediately afterwards. Simultaneous breast-feeding saves time and also has a physiologic advantage in that the more vigorous baby on one side may stimulate the letdown reex for the other twin [52]. However, the most common practice is to start breast-feeding each baby individually since it takes time for the mother to recover from the delivery, the infants do not necessarily have the same sucking ability and the new situation is often quite overwhelming for the parents. Many mothers and infants adapt rapidly and can soon choose their preferred schedule.

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Figure 2. Mother feeding twins in the double cradle position.

Figure 3. Mother feeding twins in the combination position.

3. Combination of cradle with football One infant is held in the cradle position and the second in the football position (see Fig. 3). Mothers of triplets or quadruplets who intend to provide their infants with some exposure to human milk may choose between the various possible combinations. It is probably true that even partial breast-feeding may offer potential advantages to high multiples.

Obstacles to success The mothers of multiple are often faced with additional obstacles to success in lactation. A high percentage of multiples are delivered by Caesarean section and many are born prematurely and suffer perinatal complications. These factors may have deleterious effects on breast-feeding. For example, infants delivered by Caesarean section

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start suckling later than those born by vaginal delivery [55]. Preterm multiples are at particularly high risk for neonatal complications, congenital anomalies and maternalinfant separation in the postpartum period that can also jeopardize the successful onset of breast-feeding. Breast-feeding after Caesarean section Breast-feeding multiples after a Caesarean section is not a simple task. Epidural or spinal anaesthesia is preferable in allowing the mother to be awake and relatively pain-free in the immediate post-operative period. This may improve the chances for early initiation of breast-feeding. For some mothers, the best position for breast-feeding after surgery is the football position since the babies will not lie on the mothers abdomen. Others may put a cushion over the incision to reduce the pain. Mothers of multiples report a delay in copious milk production, and thus much support and encouragement are required during the rst few days after birth. Appropriate pain relief may aid during this period. However, the compatibility of all drugs with lactation should be carefully checked before prescription [55].

the frequent trials and tribulations which are part of the potentially profound experience of breast-feeding multiples. Finally, it must be remembered despite the many potential advantages of breast-feeding multiples, this is a difficult and stressful challenge which should be approached with appropriate sensitivity and understanding.

Websites for the parents of multiples

There are many of websites that focus on either breast-feeding or multiple pregnancies. The following sites provide useful information on these two issues. www.lalecheleague.org/bfmultiple.html www.tripletconnection.org/bbfeed.html  www.dhs.vic.gov.au/phd/hce/hwu/breast/ breast.htm  www.tqq.com/supportnetwork.html
 

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Small, preterm multiples may benet from expressed breast milk until they are capable of actively breast-feeding at around 3034 weeks. This process requires much support from a multidisciplinary team in the neonatal intensive care unit [56].

Concluding remarks
Human milk is the best available source of nutrition for singletons and multiples alike. Mothers are capable of producing enough milk for more than one infant. In order that multiples should obtain maximum benet from this natural resource, mothers need much support and guidance. This may include nutritional and other advice during pregnancy and lactation and intensive support during the early stages of establishment of breast-feeding. In addition, many mothers require assistance during

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