Skip to main content

Complementary feeding in preterm infants: a position paper by Italian neonatal, paediatric and paediatric gastroenterology joint societies

Abstract

Nutrition in the first 1000 days of life is essential to ensure appropriate growth rates, prevent adverse short- and long-term outcomes, and allow physiologic neurocognitive development. Appropriate management of early nutritional needs is particularly crucial for preterm infants. Although the impact of early nutrition on health outcomes in preterm infants is well established, evidence-based recommendations on complementary feeding for preterm neonates and especially extremely low birth weight and extremely low gestational age neonates are still lacking. In the present position paper we performed a narrative review to summarize current evidence regarding complementary feeding in preterm neonates and draw recommendation shared by joint societies (SIP, SIN and SIGENP) for paediatricians, healthcare providers and families with the final aim to reduce the variability of attitude and timing among professionals.

Main text

Introduction

Nutrition in the first 1000 days of life can help ensure appropriate growth rates and prevent adverse short- and long-term outcomes in infants [1]. Early nutrition is also essential for physiologic neurocognitive development [2,3,4]. Appropriate management of early nutritional needs is particularly crucial for preterm infants, a vulnerable population that features specific nutritional requirements which differ from those of term neonates [5]. Prematurity (defined as birth before 37 weeks gestational age [GA]) still affects 7–11% of live births worldwide every year [6, 7] and it represents a significant cause of mortality and morbidity not only in the first years of life, but also later in life. Premature infants frequently develop postnatal growth retardation [8] and feature an altered body composition [9, 10], with reduced fat free mass and increased adiposity [9,10,11,12].

Although the impact of early nutrition on health outcomes in preterm infants is well established, evidence-based recommendations on complementary feeding (CF) for preterm neonates and especially for extremely low birth weight (ELBW) and extremely low gestational age neonates (ELGAN) are still lacking. CF (also called weaning) is defined by the World Health Organization as “the process starting when breast milk alone is no longer sufficient to meet the nutritional requirements of infants” so that “other foods and liquids are needed, along with breast milk” [13]. It plays a pivotal role in infantile nutrition and neurodevelopment, and represents a delicate period in which either nutritional deficits or overfeeding may be exacerbated.

What is known is that guidelines for CF in term infants [14, 15] are not appropriate for preterm neonates, hence the urgency for specific recommendation for premature babies [3, 16, 17].

The objective of this position paper is to summarize current evidence regarding CF in preterm neonates and provide recommendation shared by joint societies (Italian Paediatric Society - SIP, Italian Society of Neonatology - SIN, and Italian Society of Paediatric Gastroenterology, Hepatology and Nutrition - SIGENP) for paediatricians, healthcare providers and families with the final aim to reduce the variability of attitude [18] and timing [19] among professionals.

Who is it for?

  • Paediatricians and healthcare providers involved in the care of preterm neonates and preterm infants

  • Parents and carers of preterm neonates and preterm infants

Materials and methods

A recommendation development committee was created including neonatologists, paediatricians and nutrition experts. Parent representatives were also surveyed at multiple points during the process.

The target population was determined to be preterm neonates (GA < 37 weeks) and committee members were assigned topics based on expertise.

For each topic, screening was performed according to Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines [20]. The following keywords and Mesh terms were employed: complementary food; complementary feeding; weaning; introduction; timing; preterm newborn; premature; preterm infants; health outcome; development; adiposity rebound; paediatric obesity; body mass index; nutrition; post-discharge formula; macronutrients; oral dysfunction; allergy; “Weaning”[Mesh]; “Infant, newborn”[Mesh]; “Diet, vegetarian”[Mesh]; “Diet, vegan” [Mesh]. Proper Boolean operators “AND” and “OR” were also included to be as comprehensive as possible. Search limits were set for studies published up to 31st August 2021 in English language. Eligible studies were retrieved using the PubMed, Embase, Cochrane Library and Web of Science databases. Additional studies were identified from conference proceedings, trial registries and the reference lists of the selected papers. As a result, 62 manuscripts were selected for this position paper, including 8 systematic reviews [3, 18, 21,22,23,24,25,26], 8 narrative reviews [27,28,29,30,31,32,33,34], 27 observational studies [19, 35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60], 4 controlled trials [61,62,63,64], 1 case report [65], 3 commentaries [66,67,68], 1 operational protocol [69], 3 reports [70,71,72], 1 consensus [73], 2 recommendations [74, 75], 2 guidelines [76, 77] and 3 nutritional reference values [78,81,80]. One or more recommendations/statements were drafted for each topic. Grading of Recommendations, Assessment, Development and Evaluation (GRADE) approach [81] was used to assess the quality of evidence (i.e., high, moderate, low or very low) and to define the strength of the recommendations (i.e., weak or strong) according to potential desirable and undesirable consequences of the recommendation. Final recommendations and statements were reviewed by experts and future guideline users to ensure feasibility. Based on available data, recommendations and statements were proposed, discussed and rephrased until a consensus of 90% or more was reached.

When should complementary feeding be started?

The timing for introduction of solid foods in preterm infants is still a matter of debate. Different timeframes were suggested in the past such as 3–6 months of postnatal age (PA) [70, 71], 5–8 months of PA [72, 76] or more recently from 3 months of corrected age (CA) [18].

The majority of data on CF in preterm infants were derived from observational studies, thus reducing the robustness of the recommendations. Only few randomized controlled trials have assessed differences between timings of CF introduction (Table 1). Marriott et al. divided 68 preterm infants in two groups: “preterm weaning strategy (PWS)” group or control group. The PWS group was weaned at 13 weeks of age and at least 3.5 kg body weight compared to 17 weeks of age and at least 5 kg. The PWS group also received advice regarding quality of foods, encouraging the consumption of high-energy and high-protein foods, and a mixture of dried cereals and home-prepared foods with preterm infant formula. Their results show that the PWS featured greater length at 12 months of age, with no differences in weight or head circumference, compared to the control group [61]. A prospective cohort study by Spiegler et al. [35] showed in a regression analysis that length and weight of VLBW infants at 24 months were positively influenced by early introduction of CF: VLBW infants at 24 months of age were on average ~ 0.4 cm taller and 100 g heavier for each month of earlier introduction of CF. Also Rodriguez et al. found a beneficial effect of weaning before 4 months of CA with higher weight gain at 18–24 months of CA in very preterm infants [46].

Table 1 Main features of RCTs and observational studies assessing timing for CF introduction in preterm infants

Conversely, an RCT conducted in India to compare two different timings of CF (4 vs. 6 months CA) in ex preterm neonates with GA < 34 weeks revealed that weight-for-age z score at 12 months CA did not differ between groups, but the 4-month CA group experienced a higher rate of hospital admission primarily due to infectious disease [62]. Hence authors recommend to delay CF until 6 months CA in this population, however generalisability of their findings is uncertain due to the important differences between low and high income countries, including higher mortality rate, environmental conditions, and predominantly vegetarian dietary regimens [68].

Similarly, a pooled analysis of prospective studies by Morgan et al. [21] showed no effects on height and weight at 24 months of age and health outcomes up to 18 months.

What is known is that preterm infants are usually weaned early (before 4 months of age) compared to their term counterpart [3, 54,55,56,57]. Moreover, the first solid food is often nutritionally inadequate, with a low energy and protein content [56], and wide variability in weaning practices and vitamin and iron supplementations [19]. The entity of prematurity influences greatly the timing of weaning: preterm infants born at 22–32 weeks GA show a 9.90 odds of receiving CF before 4 months of age, compared to term peers [58].

However, also late preterm infants are often weaned early, at a mean postnatal age of 5.7 months and a mean CA of 4.6 months [59].

The early introduction of solid foods in preterm infants has been linked to a higher risk of rapid weight gain [46], allergy and anaemia whilst a delayed weaning (after 7–10 months of PA) may increase the risk of avoidance feeding behaviour [18].

It is noticeable not only that preterm infants are introduced early to CF, but also that the attitude of primary care paediatricians is widely variable in terms of timing of introduction and type of suggested foods [19].

This is partly due to the lack of specific guidelines on CF introduction for preterm infants [22]. The COMA report in 1994 suggested weaning preterm infants with a body weight of at least 5 kg, provided they had acquired a few specific developmental milestones [72]. However, these suggestions may lead to a significant delay in some populations of preterm infants (e.g., ELGAN or ELBW) which would reach such criteria well beyond the timeframe (4–6 months of age) recommended by the ESPGHAN to start CF in term infants [14]. Preterm infants starting CF often show defensive behaviours at mealtime, such as refusal to open the mouth, food selectivity and feeding refusal [60]. More recently, it has been recommended that CF in preterm infants should be started between 5 and 8 months of chronological age [76] when neurodevelopmental skills (e.g. good control of the neck, disappearance of the protrusion reflex of the tongue, the reduction of reflexive suck in favour of lateral tongue movements, and the gradual appearance of lip seal) and readiness to explore new textures and flavours should have been reached by the vast majority of ex preemies. Since an adequate motor development is a pivotal requirement for starting CF, it has also been advised to consider CA in the assessment of the optimal timing for weaning preterm infants. In this respect the limit of 3 months CA has been set to ensure the acquisition of developmental skills which allow the consumption of solid foods. Importantly, CA would be a unifying criterion for the heterogeneous population of preterm infants, since it is applicable to babies of all gestational ages, from the lowest to the highest [3].

Although critical, neurodevelopmental readiness is not the only aspect to take into consideration. Difficult transition to complementary food may also be related to comorbidities, or even behavioural issues, which should be carefully assessed with the aid of a multidisciplinary team. Indeed, the multiple and unpleasant procedures undergone during hospital admission (e.g., orogastric/nasogastric tube feeding, suctioning, intubation) may lead to a negative attitude towards CF. Furthermore, parental emotional factors should not be underestimated, particularly in growth-restricted infants, whose growth rate is often concerning for parents [36, 60].

Currently, there is insufficient evidence to draw final conclusions regarding a specific timing for starting CF in preterm infants, due to their extreme variability in achieving neurodevelopmental and oral skills. Hence, we suggest an individualized approach based on the accurate evaluation of the infant development and attitude towards semi-solid foods, employing corrected or postnatal age as an indicative reference rather than a mandatory schedule.

Recommendations/Statements

  • CF in preterm infants should be started between 5 and 8 months of chronological age.

  • Consider also the limit of 3 months CA to ensure the acquisition of developmental skills which allow the consumption of solid foods.

Certainty of evidence: Moderate.

Grade of recommendation: Strong.

Are there specific recommendations for preterm infants with oral dysfunction or comorbidities?

Oral dysfunction is not uncommon among infants born preterm, due to the higher occurrence of comorbidities (e.g., bronchopulmonary dysplasia) or neurodevelopmental impairment [27, 37]. Reportedly, over 15% of preterm infants require enteral tube feeding upon discharge [38]. Lower gestational ages at birth (below 30 weeks) and neonatal surgery have been described as risk factors for oro-motor feeding problems at 12 months’ CA [39]. This sub-group of infants often features greater defensive behaviours at mealtime when starting CF, e.g. refusal to open the mouth, feeding refusal and food selectivity [60].

However, guidelines regarding CF for preterm infants with oral dysfunction or major comorbidities are still lacking, hence the nutritional strategy for these infants should be tailored and revised regularly (Table 2). Seemingly, a greater amount of food is consumed by preterm infants using a spoon-assisted mode of feeding [63], probably due to the decreased gag reflex elicited by the introduction of food with higher texture [28]. CF may be started at 3–4 months of corrected GA, encouraging the consumption of thicker foods which may be swallowed more easily.

Table 2 Main features of trials and observational studies assessing preterm infants with oral dysfunction or comorbidities

Importantly, preterm infants with oral dysfunctions or comorbidities require a multidisciplinary follow up encompassing nutrition experts, speech therapists, and a behavioural psychologist [28, 29, 69]: oro-motor stimulation should be started early for infants on prolonged tube feeds. Infants with gastrointestinal issues should also be followed up by a paediatric gastroenterologist. Ex preemies with bronchopulmonary dysplasia should be weaned with low salt, limited volume, and high energy diets; these infants usually better tolerate foods given by spoon since they may suffer from mild hypoxic spells when suckling liquids.

Complete foods based on amino-acid mixtures concentrate in small volumes a high macronutrients content: they may be an option to meet the high nutritional requirements of infants with comorbidities or of those infants unable to ingest large quantities of food [3].

Recommendations/Statements

  • Preterm infants with oral dysfunctions or comorbidities may require a multidisciplinary assessment to evaluate when and how CF should be started.

Certainty of evidence: Low.

Grade of recommendation: Weak.

Which type of food should be recommended?

When it comes to solid foods for preterm infants, two critical aspects should be taken in consideration. Firstly, if the acceptance and consumption of semi-solid food is still inadequate, attention should be paid to the intake of micronutrients. In this respect, supplementation with iron and multivitamin products are helpful to ensure the correct supply of micronutrients. Secondly, if catch-up growth has not been reached by the time of weaning, a high protein and energy intake should be promoted by means of the correct formula or specific foods to propose. The choice of the right formula milk (i.e., post-discharge or standard formula) is also dependent on the milk tolerance of the infant, since less mature preterm infants may have immature feeding skills but higher energy requirements [3, 30].

Importantly, several figures are involved in the process of weaning a preterm infant: families, primary care paediatricians and nutrition experts. Each figure plays an important role. The family is pivotal since it represents the main support for the babies and their parents. According to a recent systematic review, nutrition education for families may decrease the risk of undernutrition in term infants [23], hence we may speculate that the same could occur with ex-preemies. The primary care paediatrician should carefully evaluate growth patterns and ensure adequate adherence to prescriptions and nutritional advice. Lastly, the nutritional expert should guide all the weaning process by carefully evaluating the infant nutritional needs and neurodevelopmental and oral skills, in order to provide tailored recommendations.

More specific recommendations for preterm infants regarding type of foods to choose, sequence and speed of introduction are lacking, hence guidelines for term infants currently remain the gold standard [14]. Importantly, the beginning of CF is associated with significant changes in both macronutrients and micronutrients intake, with the risk of nutritional imbalances. The energy requirement differs according to the degree of prematurity. Embleton et al. [40] showed that preterm infants often fail to meet their dietary intake (energy 102 kcal/kg/day; protein 3.0 g/kg/day) since the first days of life and that such deficits are not recovered by the time of discharge.

Recently, Salvatori et al. [24] suggested intake of macronutrients for preterm infants taking into account recommendations conceived by The Italian Society of Human Nutrition with LARNs (Reference intake Levels of Nutrients and energy for the Italian population) of 2014 [78], the Dietary Reference Values for nutrients of European Food Safety Authority (EFSA) of 2017 [79] and the Nutrient Reference Values for Australia and New Zealand Including Recommended Dietary Intakes of 2017 [80] (Table 3).

Table 3 Macronutrients adequate intake for infants

As for micronutrients, iron supply is a matter of concern due to its essential role for brain development. Iron supplementation is recommended for preterm infants until at least 6–12 months of age [66]. However, from 6 months of age the supplementation alone would not be sufficient to provide the adequate amount of iron, hence the consumption of foods rich in iron (e.g., meat, iron-fortified cereals, fish) should be encouraged.

Recommendations/Statements

  • Recommendations for preterm infants regarding type of foods to choose, sequence and speed of introduction may be considered the same as for term infants currently.

  • Consider starting CF encompassing sources of carbohydrates, proteins and vegetable fats (extra-virgin olive oil) and paying special attention to the intake of micronutrients (e.g., iron and vitamins).

Certainty of evidence: Low.

Grade of recommendation: Weak.

Is there a link between early CF and obesity?

Extrauterine growth retardation is very frequent in preterm infants that usually weigh significantly less than expected at hospital discharge and often remain small throughout infancy and childhood. However, an excessive protein supply in the first stages of life and the early introduction of CF have been linked to increased concentrations of insulin and insulin-like growth factor-1 (IGF-1), which in turn cause higher weight gain and body fat deposition leading to an increased risk of obesity. Singhal et al. demonstrated that ex-preterm patients aged 13–16 years featured higher fasting 32–33 split proinsulin concentrations if fed with a nutrient-enriched diet in early childhood (mean 7.2 pmol/l, 95% CI 6.4–8.1 vs 5.9 pmol/l 95% CI 5.2–6.4; p = 0.01). Fasting 32–33 split proinsulin levels were also associated with greater weight gain in the first two weeks of life, suggesting that early relative undernutrition in children born preterm may have beneficial effects on insulin resistance [64].

Hence, there is still uncertainty whether the early introduction of CF is more beneficial in short-term weight gain or, in contrast, it is more detrimental due to the long-term risk of obesity and metabolic syndrome [77].

A few studies explored the influence of early weaning on body mass index (BMI) in preterm infants (Table 4). Gupta et al. did not find any significant difference of BMI index z score at 12 months according to timing of CF [62], whereas Sun et al. showed that early CF introduction was negatively associated to BMI at 12 months of age [41]. In contrast, Morgan et al. showed that preterm infants weaned before 3 months CA featured a greater gain in the subscapular skinfold thickness between 3 and 9 months CA [21].

Table 4 Main features of RCTs and observational studies assessing the relationship between CF introduction in infants and later onset of obesity

A recent study showed that half of preterm infants featured an early adiposity rebound (≤ 4 years of age) irrespective of timing of CF introduction [42], hence authors concluded that premature birth can be regarded as an independent risk factor for obesity and other non-communicable diseases later in life [25, 43]. The risk of being overweight or obese in early childhood is higher for small for gestational age (SGA) [31] and large for gestational age (LGA) [44, 45] neonates. An observational cohort study concluded that starting CF before 26 weeks of CA is associated with a higher BMI at 12 months of age in preterm infants [47]. Nonetheless, a recent systematic review regarding the link between the timing of CF in preterm infants and the incidence of overweight could not draw final conclusions due to the shortage of randomized controlled trials [26] and recent findings from a multicentre retrospective cohort study on 911 preterm infants demonstrated no associations between overweight or obesity at 3 years of age and risk factors such as extremely preterm infants being SGA or experiencing extrauterine growth retardation (EUGR) [48]. We could speculate that these contrasting findings might be due to either heterogeneity of study designs or different energy intakes between the periods of assessment.

Recommendations/Statements

  • Timing of CF start in preterm infants is unlikely to influence the incidence of overweight and obesity in childhood and adulthood.

  • The start of CF in preterm infants should not be delayed with the aim to prevent overweight and obesity.

Certainty of evidence: Moderate.

Grade of recommendation: Strong.

Is there a link between early CF and allergy?

The retrospective case-control study by Yrjänä and coll. showed that very early introduction of CF does not affect the incidence of allergy or atopic manifestations among preterm infants, suggesting that their gut-associated lymphoid tissue is ready for CF within 3 to 6 months of chronological age, regardless of GA at birth [49].

Conversely, Morgan et al. showed that preterm infants introduced early (within 17 weeks' CA) to at least four solid foods featured a higher risk of eczema in infancy [50] (Table 5). Despite limited evidence, a recent systematic review suggested that gluten and allergenic foods introduction should not be delayed in preterm infants starting CF. Gluten and allergenic foods should be offered any time after 4 months of CA, irrespective of infants’ relative risk of developing allergy. Limiting the amount of gluten during infancy might be desirable [74].

Table 5 Main features of observational studies assessing the relationship between CF introduction in preterm infants and later onset of allergy

Recommendations/Statements

  • The introduction of allergenic foods (e.g., eggs, fish, tomato, peanuts) may not be delayed in preterm infants.

Certainty of evidence: Very Low.

Grade of recommendation: Weak.

Are vegetarian and vegan weaning regimens feasible in preterm infants?

Vegetarian and vegan diets are increasingly popular [32] also among parents who are reported to ask their paediatricians for alternative weaning regimens with significant frequency [51, 52]. Paediatricians often are not prone to support parents in their decision mainly for the concerns regarding safety of alternative weaning regimens. Indeed, scientific societies [14, 75] encourage weaning regimens based on a large variety of foods and stand against alternative weaning methods due to the risk of nutritional deficiencies and long-term detrimental effects (e.g., failure to thrive, rickets, irreversible cognitive deficits, death). Alarmingly, the sceptical approach of paediatricians jeopardizes the alliance with parents [51, 65] who prefer to adhere to alternative diets with scarce guidance from healthcare professionals, whereas the collaboration between parents, paediatricians and dieticians should be strongly advocated to ensure both a comprehensive growth and development assessment, and an accurate diet planning.

Due to the shortage of consistent data supporting the safety and feasibility of alternative weaning regimens (Table 6), they should be carefully planned for preterm infants, who are a rather delicate population [52]. Parents strongly willing to adhere to alternative weaning regimens should be guided in the process by nutritional experts.

Table 6 Main features of studies assessing vegetarian and vegan weaning regimens

Consumption of foods low in fibre and rich in calcium, iron, zinc, iodine, and DHA together with the supplementation of vitamin D and B12 (in case of vegan diet) are recommended [52]. Infants should also be carefully assessed and monitored for sign and symptoms of nutritional deficits.

Recommendations/Statements

  • Vegetarian and vegan weaning may be carefully planned in preterm infants.

Certainty of evidence: Very Low.

Grade of recommendation: Weak.

Which milk should be consumed during CF?

Similarly to in-hospital nutrition, also at home the main options are human milk (HM), raw or fortified, and formula milk adapted for preterm infants. Despite the fact that fortified HM may help ensure adequate growth [33, 53], the use of fortifiers at home may be troublesome, hence parents should be carefully informed on the importance of continuing fortification after discharge from hospital to improve growth and support breastfeeding, [73] in a period when feeding and sucking competency on the breast are usually improved [53]. Hence, mother’s milk supplementation is often discontinued, exposing the infant to the risk of nutritional deficits and decreased weight gain soon after discharge [34, 53]. Whether exclusive breastfeeding at discharge and suboptimal initial weight gain in preterm infants increase the odds of later cognitive impairment is still matter of debate [1, 53]. The so-called “apparent breastfeeding paradox” clearly describes that very preterm infants started on breast milk early in the course of their life may feature better neurodevelopmental outcomes in spite of suboptimal initial weight gain, thus encouraging the use of breastfeeding in preemies [53].

According to ESPGHAN, exclusive breastfeeding, mixed feeding (in case of insufficient amounts of breast milk) or standard infant formula enriched with LCPUFA should be preferred for infants without EUGR. In contrast, in case of EUGR or high risk of long-term growth failure, infants should be fed up to 40 (but possibly 52) weeks' postmenstrual age with fortified HM or formula milk adapted for preterm infants featuring high protein contents, calcium, phosphorus, zinc, and LCPUFA [67].

Recommendations

  • Infants without EUGR may be fed with exclusive breastfeeding, mixed feeding (in case of insufficient amounts of breast milk) or standard infant formula enriched with LCPUFA.

  • Infants with EUGR or at high risk of long-term growth failure may be fed with fortified HM or formula milk adapted for preterm infants as long as necessary to gain an optimal weight for CA.

Evidence quality: Low.

Grade of recommendation: Weak.

Conclusions

To the best of our knowledge, the present position paper by joint societies (SIP, SIN and SIGENP) is the first to draw tailored guidance regarding nutrition and complementary feeding of preterm infants.

We suggest that CF in preterm infants should be started between 5 and 8 months of chronological age, taking also into account the limit of 3 months CA to ensure the acquisition of crucial neurodevelopmental skills which allow the consumption of solid foods. As for type of foods to choose, sequence and speed of introduction, the same guidelines available for term infants should be applied also for ex-preemies. CF should be started encompassing sources of carbohydrates, proteins and vegetable fats (although whether a specific type of vegetable fat should be preferred is still unknown). Attention should be paid to the intake of micronutrients (e.g., iron and vitamins).

A multidisciplinary assessment to evaluate when and how CF should be started is recommended for preterm infants with oral dysfunctions or comorbidities.

According to current knowledge, the timing of CF in preterm infants is unlikely to influence the incidence of overweight and obesity in childhood and adulthood. Thus, it is not necessary to delay the start of CF in preterm infants to prevent overweight and obesity. Similarly, the introduction of allergenic foods (e.g., eggs, fish, tomato, peanuts) should not be delayed in preterm infants.

Vegetarian and vegan weaning should be carefully planned in preterm infants, in order to prevent detrimental effects due to nutritional deficiencies.

Future research should also aim at providing tailored recommendations for subgroups of preterm infants, such as late preterm neonates, that feature higher risk of lower weight and height during childhood, insulin resistance, glucose intolerance, and high blood pressure compared to term neonates, and whose nutritional requirements are still matter of debate [82].

Availability of data and materials

All relevant data are included in the article.

Abbreviations

AGA:

Appropriate for gestational age

BMI:

Body mass index

BW:

Birth weight

CA:

Corrected age

CF:

Complementary feeding

DHA:

Docosahexaenoic acid

EFSA:

European Food Safety Authority

ELBW:

Extremely low birth weight

ELGAN:

Extremely low gestational age neonates

EUGR:

Extrauterine growth retardation

GA:

Gestational age

GRADE:

Grading of Recommendations, Assessment, Development and Evaluation

HM:

Human milk

IGF-1:

Insulin-like growth factor-1

IUGR:

Intrauterine growth restriction

LARNs:

Reference intake Levels of Nutrients

LCPUFA:

Long-chain polyunsaturated fatty acids

LGA:

Large for gestational age

OFP:

Oral feeding protocol

PA:

Postnatal age

PRISMA:

Preferred Reporting Items for Systematic Review and Meta-Analysis

PWS:

Preterm weaning strategy

RCT:

Randomized controlled trial

SGA:

Small for gestational age

SIGENP:

Italian Society of Paediatric Gastroenterology, Hepatology and Nutrition

SIN:

Italian Society of Neonatology

SIP:

Italian Society of Paediatrics

References

  1. Haschke F, Binder C, Huber-Dangl M, Haiden N. Early-life nutrition, growth trajectories, and long-term outcome. Nestle Nutr Inst Workshop Ser. 2019;90:107–20.

    PubMed  Article  Google Scholar 

  2. Schwarzenberg SJ, Georgieff MK, COMMITTEE ON NUTRITION CO. Advocacy for improving nutrition in the first 1000 days to support childhood development and adult health. Pediatrics. 2018;141(2):e20173716. https://doi.org/10.1542/peds.2017-3716.

    Article  PubMed  Google Scholar 

  3. Liotto N, Cresi F, Beghetti I, Roggero P, Menis C, Corvaglia L, et al. Complementary feeding in preterm infants: a systematic review. Nutrients. 2020;12:1–13.

    Google Scholar 

  4. Kumar RK, Singhal A, Vaidya U, Banerjee S, Anwar F, Rao S. Optimizing nutrition in preterm low birth weight infants—consensus summary. Front Nutr. 2017;4:20.

    PubMed  PubMed Central  Article  Google Scholar 

  5. Riskin A. Meeting the nutritional needs of premature babies: their future is in our hands. Br J Hosp Med. 2017;78:690–4.

    Article  Google Scholar 

  6. Harrison MS, Goldenberg RL. Global burden of prematurity. Semin Fetal Neonatal Med. 2016;21:74–9.

    PubMed  Article  Google Scholar 

  7. Purisch SE. Epidemiology of preterm birth. Semin Perinatol. 2017;41:387–91.

    PubMed  Article  Google Scholar 

  8. Cooke RJ. Improving growth in preterm infants during initial hospital stay: principles into practice. Arch Dis Child Fetal Neonatal Ed. 2016;101:F366–70.

    PubMed  Article  Google Scholar 

  9. Roggero P, Giannì ML, Amato O, Orsi A, Piemontese P, Morlacchi L, et al. Is term newborn body composition being achieved postnatally in preterm infants? Early Hum Dev. 2009;85:349–52.

    PubMed  Article  Google Scholar 

  10. Giannì ML, Roggero P, Liotto N, Taroni F, Polimeni A, Morlacchi L, et al. Body composition in late preterm infants according to percentile at birth. Pediatr Res. 2016;79:710–5.

    PubMed  Article  Google Scholar 

  11. Ramel SE, Gray HL, Christiansen E, Boys C, Georgieff MK, Demerath EW. Greater early gains in fat-free mass, but not fat mass, are associated with improved neurodevelopment at 1 year corrected age for prematurity in very low birth weight preterm infants. J Pediatr. 2016;173:108–15.

    PubMed  Article  Google Scholar 

  12. Parlapani E, Agakidis C, Karagiozoglou-Lampoudi T. Anthropometry and body composition of preterm neonates in the light of metabolic programming. J Am Coll Nutr. 2018;37:350–9.

    PubMed  Article  Google Scholar 

  13. World Health Organization. Complementary feeding: report of the global consultation, and summary of guiding principles for complementary feeding of the breastfed child. World Health Organization. 2003. https://apps.who.int/iris/handle/10665/42739.

  14. Fewtrell M, Bronsky J, Campoy C, et al. Complementary feeding: a position paper by the European Society for Paediatric Gastroenterology, hepatology, and nutrition (ESPGHAN) committee on nutrition. J Pediatr Gastroenterol Nutr. 2017;64:119–32.

    CAS  PubMed  Article  Google Scholar 

  15. Alvisi P, Brusa S, Alboresi S, et al. Recommendations on complementary feeding for healthy, full-term infants. Ital J Pediatr. 2015;41:36.

    PubMed  PubMed Central  Article  Google Scholar 

  16. Baldassarre ME, Giannì ML, Di Mauro A, Mosca F, Laforgia N. Complementary feeding in preterm infants: where do we stand? Nutrients. 2020;12:1259.

    PubMed Central  Article  Google Scholar 

  17. Barachetti R, Villa E, Barbarini M. Weaning and complementary feeding in preterm infants: management, timing and health outcome. La Pediatr Medica e Chir. 2017;39(4):181. https://doi.org/10.4081/pmc.2017.181.

    Article  Google Scholar 

  18. Palmer DJ, Makrides M. Introducing solid foods to preterm infants in developed countries. Ann Nutr Metab. 2012;60:31–8.

    CAS  PubMed  Article  Google Scholar 

  19. Baldassarre ME, Di Mauro A, Pedico A, Rizzo V, Capozza M, Meneghin F, et al. Weaning time in preterm infants: an audit of italian primary care paediatricians. Nutrients. 2018;10:616.

    PubMed Central  Article  Google Scholar 

  20. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.

    PubMed  PubMed Central  Article  Google Scholar 

  21. Morgan JB, Lucas A, Fewtrell MS. Does weaning influence growth and health up to 18 months? Arch Dis Child. 2004;89:728–33.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Castenmiller J, de Henauw S, Hirsch-Ernst KI, et al. Appropriate age range for introduction of complementary feeding into an infant’s diet. EFSA J. 2019;17:e05780.

    PubMed  PubMed Central  Google Scholar 

  23. Ojha S, Elfzzani Z, Kwok TC, Dorling J. Education of family members to support weaning to solids and nutrition in later infancy in term-born infants. Cochrane Database Syst Rev. 2020;7(7):CD012241. https://doi.org/10.1002/14651858.CD012241.pub2.

    Article  PubMed  Google Scholar 

  24. Salvatori G, Martini L, Neonatology the SG on NN and GS of. Complementary feeding in the preterm infants: summary of available macronutrient intakes and requirements. Nutrients. 2020;12:3696.

    CAS  PubMed Central  Article  Google Scholar 

  25. Llewellyn A, Simmonds M, Owen CG, Woolacott N. Childhood obesity as a predictor of morbidity in adulthood: a systematic review and meta-analysis. Obes Rev. 2016;17:56–67.

    CAS  PubMed  Article  Google Scholar 

  26. Vissers KM, Feskens EJM, van Goudoever JB, Janse AJ. The timing of initiating complementary feeding in preterm infants and its effect on overweight: a systematic review. Ann Nutr Metab. 2018;72:307–15.

    CAS  PubMed  Article  Google Scholar 

  27. Lau C. Development of infant oral feeding skills: what do we know? Am J Clin Nutr. 2016;103:616S–21S.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. Dusick A. Investigation and Management of Dysphagia. Semin Pediatr Neurol. 2003;10:255–64.

    PubMed  Article  Google Scholar 

  29. Biniwale MA, Ehrenkranz RA. The role of nutrition in the prevention and Management of Bronchopulmonary Dysplasia. Semin Perinatol. 2006;30:200–8.

    PubMed  Article  Google Scholar 

  30. Crippa BL, Morniroli D, Baldassarre ME, Consales A, Vizzari G, Colombo L, et al. Preterm’s nutrition from hospital to solid foods: are we still navigating by sight? Nutrients. 2020;12:1–9.

    Article  Google Scholar 

  31. Dulloo AG, Jacquet J, Seydoux J, Montani JP. The thrifty ‘catch-up fat’ phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes. 2006;30:S23–35.

    CAS  Article  Google Scholar 

  32. Ferrara P, Corsello G, Quattrocchi E, Dell’Aquila L, Ehrich J, Giardino I, et al. Caring for infants and children following alternative dietary patterns. J Pediatr. 2017;187:339–340.e1.

    PubMed  Article  Google Scholar 

  33. Nzegwu NI, Ehrenkranz RA. Post-discharge nutrition and the VLBW infant: to supplement or not supplement? A review of the current evidence. Clin Perinatol. 2014;41:463–74.

    PubMed  Article  Google Scholar 

  34. Greer FR. Post-discharge nutrition: what does the evidence support? Semin Perinatol. 2007;31:89–95.

    PubMed  Article  Google Scholar 

  35. Spiegler J, Eisemann N, Ehlers S, Orlikowsky T, Kannt O, Herting E, et al. Length and weight of very low birth weight infants in Germany at 2 years of age: does it matter at what age they start complementary food? Eur J Clin Nutr. 2015;69:662–7.

    CAS  PubMed  Article  Google Scholar 

  36. Crapnell TL, Rogers CE, Neil JJ, Inder TE, Woodward LJ, Pineda RG. Factors associated with feeding difficulties in the very preterm infant. Acta Paediatr Int J Paediatr. 2013;102:e539–45.

    CAS  Article  Google Scholar 

  37. Pahsini K, Marinschek S, Khan Z, Urlesberger B, Scheer PJ, Dunitz-Scheer M. Tube dependency as a result of prematurity. J Neonatal Perinatal Med. 2018;11:273–9.

    Article  Google Scholar 

  38. Kamitsuka MD, Nervik PA, Nielsen SL, Clark RH. Incidence of nasogastric and gastrostomy tube at discharge is reduced after implementing an Oral feeding protocol in premature (< 30 weeks) infants. Am J Perinatol. 2017;34:606–13.

    PubMed  Article  Google Scholar 

  39. Sanchez K, Spittle AJ, Slattery JM, Morgan AT. Oromotor feeding in children born before 30 weeks’ gestation and term-born peers at 12 months’ corrected age. J Pediatr. 2016;178:113–118.e1.

    PubMed  Article  Google Scholar 

  40. Embleton ND, Pang N, Perring J, Cooke RJ. Systematic underfeeding of preterm infants on neonatal intensive care units. Pediatr Res. 1999;45:281A.

    Article  Google Scholar 

  41. Sun C, Foskey RJ, Allen KJ, et al. The impact of timing of introduction of solids on infant body mass index. J Pediatr. 2016;179:104–110.e1.

    PubMed  Article  Google Scholar 

  42. Baldassarre ME, Di Mauro A, Caroli M, Schettini F, Rizzo V, Panza R, et al. Premature birth is an independent risk factor for early adiposity rebound: longitudinal analysis of bmi data from birth to 7 years. Nutrients. 2020;12:1–11.

    Google Scholar 

  43. Baldassarre ME, Di Mauro A, Cintoli A, Mincarone G, Tafuri S, Laforgia N. Non-communicable chronic diseases: the role of neonatal characteristics. Iran J Pediatr. 2017;27:e9322.

    Google Scholar 

  44. Kaul P, Bowker SL, Savu A, Yeung RO, Donovan LE, Ryan EA. Association between maternal diabetes, being large for gestational age and breast-feeding on being overweight or obese in childhood. Diabetologia. 2019;62:249–58.

    CAS  PubMed  Article  Google Scholar 

  45. Kapral N, Miller SE, Scharf RJ, Gurka MJ, DeBoer MD. Associations between birthweight and overweight and obesity in school-age children. Pediatr Obes. 2018;13:333–41.

    CAS  PubMed  Article  Google Scholar 

  46. Rodriguez J, Affuso O, Azuero A, Downs CA, Turner-Henson A, Rice M. Infant feeding practices and weight gain in toddlers born very preterm: a pilot study. J Pediatr Nurs. 2018;43:29–35.

    PubMed  Article  Google Scholar 

  47. Brion LP, Rosenfeld CR, Heyne R, Steven Brown L, Lair CS, Heyne E, et al. Association of age of initiation and type of complementary foods with body mass index and weight-for-length at 12 months of age in preterm infants. J Perinatol. 2020;40:1394–404.

    PubMed  Article  Google Scholar 

  48. Fenton TR, Nasser R, Creighton D, Elmrayed S, Tang S, Gillis C, et al. Critical examination of relationships between early growth and childhood overweight in extremely preterm infants. J Perinatol. 2021;41:2774–81.

    PubMed  Article  Google Scholar 

  49. Yrjänä JMS, Koski T, Törölä H, Valkama M, Kulmala P. Very early introduction of semisolid foods in preterm infants does not increase food allergies or atopic dermatitis. Ann Allergy Asthma Immunol. 2018;121:353–9.

    PubMed  Article  Google Scholar 

  50. Morgan J, Williams P, Norris F, Williams CM, Larkin M, Hampton S. Eczema and early solid feeding in preterm infants. Arch Dis Child. 2004;89:309–14.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Bivi D, Di Chio T, Geri F, et al. Raising children on a vegan Diet : parents ’ opinion on problems in everyday life. Nutrients. 2021;13:1–14.

    Article  CAS  Google Scholar 

  52. Baldassarre ME, Panza R, Farella I, Posa D, Capozza M, Di Mauro A, et al. Vegetarian and vegan weaning of the infant: how common and how evidence-based? A population-based survey and narrative review. Int J Environ Res Public Health. 2020;17:1–17.

    Google Scholar 

  53. Rozé J-C, Darmaun D, Boquien C-Y, et al. The apparent breastfeeding paradox in very preterm infants: relationship between breast feeding, early weight gain and neurodevelopment based on results from two cohorts. Epipage Lift BMJ Open. 2012;2:e000834.

    PubMed  Article  Google Scholar 

  54. Zielinska MA, Rust P, Masztalerz-Kozubek D, Bichler J, Hamułka J. Factors influencing the age of complementary feeding—a cross-sectional study from two European countries. Int J Environ Res Public Health. 2019;16:3799.

    PubMed Central  Article  Google Scholar 

  55. Cleary J, Dalton SM, Harman A, Wright IM. Current practice in the introduction of solid foods for preterm infants. Public Health Nutr. 2020;23:94–101.

    PubMed  Article  Google Scholar 

  56. Fanaro S, Borsari G, Vigi V. Complementary feeding practices in preterm infants: an observational study in a cohort of Italian infants. J Pediatr Gastroenterol Nutr. 2007;45:S210–4.

    PubMed  Article  Google Scholar 

  57. Norris F, Larkin M, Williams C, Hampton S, Morgan J. Factors affecting the introduction of complementary foods in the preterm infant. Eur J Clin Nutr. 2002;56:448–54.

    CAS  PubMed  Article  Google Scholar 

  58. Braid S, Harvey EM, Bernstein J, Matoba N. Early introduction of complementary foods in preterm infants. J Pediatr Gastroenterol Nutr. 2015;60:811–8.

    PubMed  Article  Google Scholar 

  59. Giannì ML, Bezze E, Colombo L, Rossetti C, Pesenti N, Roggero P, et al. Complementary feeding practices in a cohort of Italian late preterm infants. Nutrients. 2018;10:1861.

    PubMed Central  Article  Google Scholar 

  60. Menezes LVP, Steinberg C, Nóbrega AC. Complementary feeding in infants born prematurely. CODAS. 2018;30:e20170157.

    PubMed  Article  Google Scholar 

  61. Marriott LD, Foote KD, Bishop JA, Kimber AC, Morgan JB. Weaning preterm infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2003;88:F302–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. Gupta S, Agarwal R, Aggarwal KC, et al. Complementary feeding at 4 versus 6 months of age for preterm infants born at less than 34 weeks of gestation: a randomised, open-label, multicentre trial. Lancet Glob Heal. 2017;5:e501–11.

    Article  Google Scholar 

  63. Malhotra N, Vishwambaran L, Sundaram KR, Narayanan I. A controlled trial of alternative methods of oral feeding in neonates. Early Hum Dev. 1999;54:29–38.

    CAS  PubMed  Article  Google Scholar 

  64. Singhal A, Fewtrell M, Cole TJ, Lucas A. Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet. 2003;361:1089–97.

    CAS  PubMed  Article  Google Scholar 

  65. Farella I, Panza R, Baldassarre ME. The difficult Alliance between vegan parents and pediatrician: a case report. Int J Environ Res Public Health. 2020;17:6380.

    PubMed Central  Article  Google Scholar 

  66. Agostoni C, Buonocore G, Carnielli V, et al. Enteral nutrient supply for preterm infants: commentary from the European Society of Paediatric Gastroenterology, hepatology and nutrition Committee on nutrition. J Pediatr Gastroenterol Nutr. 2010;50:85–91.

    CAS  PubMed  Article  Google Scholar 

  67. ESPGHAN Committee on Nutrition A, Aggett PJ, Agostoni C, et al. Feeding preterm infants after hospital discharge: a commentary by the ESPGHAN Committee on nutrition. J Pediatr Gastroenterol Nutr. 2006;42:596–603.

    Article  Google Scholar 

  68. Embleton ND, Fewtrell M. Complementary feeding in preterm infants. Lancet Global Health. 2017;5(5):e470–1. https://doi.org/10.1016/S2214-109X(17)30151-1.

    Article  PubMed  Google Scholar 

  69. Lipner HS, Huron RF. Developmental and Interprofessional Care of the Preterm Infant: neonatal intensive care unit through high-risk infant follow-up. Pediatr Clin N Am. 2018;65:135–41.

    Article  Google Scholar 

  70. Sleigh G, Ounsted M. Present-day practice in infant feeding. Lancet. 1975;305:753.

    Article  Google Scholar 

  71. DHSS (Department of Health and Social Security). Present day practice in infant feeding. Lancet. 1988;331:975–6.

  72. Department of Health. Weaning and the weaning diet. Rep Health Soc Subj (Lond). 1994;45:1-113.

  73. McCormick K, King C, Clarke S, Jarvis C, Johnson M, Parretti HM, et al. The role of breast milk fortifier in the post-discharge nutrition of preterm infants. Br J Hosp Med. 2021;82:42–8.

    Article  Google Scholar 

  74. Chiale F, Maggiora E, Aceti A, Liotto N, Coscia A, Peila C, et al. Complementary feeding: recommendations for the introduction of allergenic foods and gluten in the preterm infant. Nutrients. 2021;13:2477.

    PubMed  PubMed Central  Article  Google Scholar 

  75. Lemale J, Mas E, Jung C, Bellaiche M, Tounian P. Vegan diet in children and adolescents. Recommendations from the French-speaking pediatric hepatology, gastroenterology and nutrition group (GFHGNP). Arch Pediatr. 2019;26:442–50.

    CAS  PubMed  Article  Google Scholar 

  76. King C. An evidence based guide to weaning preterm infants. Paediatr Child Health (Oxford). 2009;19:405–14.

    Article  Google Scholar 

  77. Fauser B, Alikani M, Franklin S, Johnson MH, Garcia-Velasco J. A bright future. Reprod BioMed Online. 2017;34:1–2.

    PubMed  Article  Google Scholar 

  78. Società Italiana di Nutrizione Umana (SINU). LARN: Livelli di Assunzione di Riferimento di Nutrienti ed Energia. 4th ed. Milano: SICS; 2014. https://sinu.it/larn/.

  79. EFSA. Dietary Reference Values for nutrients Summary report. Support Publ. 14:e15121E.

  80. The National Health and Medical Research Council. Nutrient Reference Values for Australia and New Zealand Including Recommended Dietary Intakes. Available online: https://www.nhmrc.gov.au/about-us/publications/nutrient-reference-values-australia-and-new-zealand-including-recommended-dietary-intakes

  81. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924–6.

    PubMed  PubMed Central  Article  Google Scholar 

  82. Lapillonne A, Bronsky J, Campoy C, et al. Feeding the late and moderately preterm infant: a position paper of the European Society for Paediatric Gastroenterology, hepatology and nutrition Committee on nutrition. J Pediatr Gastroenterol Nutr. 2019;69:259–70.

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We acknowledge Dr. Alessandra Mazzocchi and Dr. Valentina De Cosmi for their contribution in revising the manuscript.

Funding

This research did not receive any specific grant from funding agencies of public, commercial, or not-for-profit sectors. Raffaella Panza received a fellowship funded by Mellin S.p.A. (Milan, Italy) to attend the Doctorate (PhD) course in Biomolecular Pharmaceutical and Medical Sciences of University of Bari - Aldo Moro.

Author information

Authors and Affiliations

Authors

Consortia

Contributions

Conceptualization, M.E.B. and R.P.; Methodology, G.S., N.Li., M.L.G., L.C., A.A., F.C., L.I.; Writing – Original Draft Preparation, R.P., M.E.B.; Writing – Review & Editing, N.La., G.S., N.Li., M.L.G., L.C., A.A., F.C., L.I., L.M., A.D.; Supervision, C.A., F.M, A.S., L.O, P.L.. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Raffaella Panza.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Baldassarre, M.E., Panza, R., Cresi, F. et al. Complementary feeding in preterm infants: a position paper by Italian neonatal, paediatric and paediatric gastroenterology joint societies. Ital J Pediatr 48, 143 (2022). https://doi.org/10.1186/s13052-022-01275-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13052-022-01275-w

Keywords

  • Nutrition
  • Complementary feeding
  • Weaning [Mesh]
  • Breastfeeding [Mesh]
  • Breast milk [Mesh]
  • Fortification
  • Infant, Premature [Mesh]
  • Preterm, Births [Mesh]