Darla Shores is an assistant professor in the Division of Pediatric Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Johns Hopkins School of Medicine. She is also the school’s medical codirector of the Intestinal Rehabilitation Program and Associate Fellowship Program director.

Darla Shores, MD, PhD

Obesity has increased in many segments of the population over recent decades, including children and adolescents. The COVID-19 pandemic has accelerated that trend, bringing to light changing patterns in eating habits, disparities in access to healthy food, decreased activity, and increased risk of poor health outcomes.

Historically, food was transformed for improved palatability, as well as preservation and storage.

 Foods have been processed to make them more appealing for both convenience and taste. Since the 1970s, ultraprocessed foods have been available in most of the world and over the past 20 years have become a major source of calories, comprising an average of 3 out of 5 calories consumed daily

). Ultraprocessed foods are easy to manufacture, which reduces industrial costs for companies.

 Food corporations have focused on advertising and marketing of these products to improve sales, but eating more ultraprocessed foods leads to a decline in dietary content of important vitamins, minerals, protein, and fiber.

Increased consumption of ultraprocessed foods has paralleled an increase in obesity, now involving low- and middle-income countries as well, contributing to a global health crisis.

 Children are an especially vulnerable population because they have higher nutritional needs for healthy growth, and critical nutrients are often absent from a diet of mostly ultraprocessed foods.

 The number of ready-to-eat meals consumed has significantly increased as well in the United States (Table 1).

 Adequate nutrition is necessary to support the immune system and prevent infection.

 Eating a diet low in nutritional value increases risk of malnutrition and rates of chronic diseases.

The NOVA classification system, developed by investigators at the University of Sao Paulo in Brazil, separates food into 4 categories based on their constitution and alteration. Foods with significant processing classically have been viewed as detrimental to overall health with promotion of weight gain and risk of chronic disease; however, there has been some discussion of the pitfalls that come with the classification system.

 Some foods are processed to add nutrients, such as iron-fortified cereal.

 Processing also may be important to ensure the safety of foods consumed.

Nevertheless, ultraprocessed foods are generally of low nutritional quality with high-energy density and are associated with the development of chronic noncommunicable diseases with long-term effects on health. Consumption of ultraprocessed foods is associated with a high glycemic response and reduced satiety, which may contribute to overeating.

 Noncommunicable chronic diseases, including cardiovascular disease and metabolic syndrome, account for 70% of deaths worldwide.

 foods consumed whole without major alterations or changes. These include fresh or frozen fruits, vegetables, meats, or legumes with minimal processing. The food itself is not changed and is considered a whole food.

 food items used in cooking to add flavor and taste or that are part of unprocessed foods. These include table salt, sugar, oil, and other substances extracted from unprocessed foods.

 foods taken from nature and altered with added substances, often sugar or salt, to create more stable and appealing foods. This includes canned fruits and vegetables, simple breads, and cheeses.

 foods with a combination of several ingredients creating a packaged food or meal that is sustainable, convenient, and appetizing. In addition to added culinary ingredients (sugar, salt, and oils), ultraprocessed foods also include nonculinary products such as high fructose corn syrup and artificial sweeteners.

 Added sugars, saturated fats, emulsifiers, and preservatives can extend the shelf life for months to years.

 Added sugars include brown sugar, cane sugar, confectioner’s sugar, granulated sugar, syrups, and honey. These foods tend to promote inflammation.

 The 2015-2020 Dietary Guidelines for Americans recommended limited intake of added sugars with a goal that sugars be less than 10% of total calories consumed.

Recent research into the dietary habits of adolescents around the world has focused on exposure to ultraprocessed foods. The National Health and Nutrition Examination Survey reviewed 10 cycles of 24-hour dietary recall to understand what children and adolescents were eating daily. They reviewed 2 different time periods, 1999-2000 and 2017-2018 to look at dietary eating habits.

 They found that consumption of ultraprocessed foods increased as children got older, with the highest percentages of daily intake occurring in adolescents.

Adolescence is a crucial time for emotional, mental, and physical development as individuals gain autonomy and independence. Several factors influence eating habits of adolescents, including their physical surroundings and social environment, self-awareness of food preferences and nutritional needs, and their exposure to the digital world of social media and advertisements.

 Adolescents believe the definition of healthy includes a balanced diet, consistent physical activity, and maintenance of a healthy body weight, but they sometimes struggle with how to characterize energy-dense and processed food.

 Food marketing targeted at children and adolescents through television and social media has been linked with a preference for those ultraprocessed foods that tend to be unhealthy.

 In 2009, $1.8 billion was spent on marketing to adolescents of ultraprocessed foods such as sugary carbonated beverages, snack foods, cookies, potato chips, and cakes.

The World Health Organization has recommended reducing advertisements targeted toward children and developing a nutritional criterion for advertising.

 Governing bodies have encouraged a reduction of targeted marking of ultraprocessed foods to children and adolescents. The Better Business Bureau’s voluntary Child Food and Beverage Initiative in 2006 promoted reduced marketing. Seventeen large corporations agreed to advertise only healthy foods to children but in the end only a few companies actually reduced their marketing.

Other governing policy changes such as a soda tax has led to a decreased consumption of soft drinks.

 The National Student Lunch Program has been modified to reduce total calories and to increase fruits and vegetables. These changes have led to a slight decrease in ultraprocessed foods available at schools, however there is still a lot left to do to improve the health of children and adolescents.

The COVID-19 pandemic disrupted dietary habits with the transition from work and school to home for many families. The pandemic heightened the consumption of ultraprocessed foods as schools closed and access to food changed.

 In the early months of the pandemic, more meals were cooked and prepared at home to allow for social distancing and infrequent trips to restaurants and stores. However, this also meant that foods with longer shelf lives and sustainability, such as high-calorie snacks and nonperishable goods, were purchased more often.

 With the economic burden of the pandemic, families attempted to cope with food insecurity by purchasing foods with long shelf lives and low cost to ensure there would be food in the house.

The environment in which food was consumed in the home also has been altered during the pandemic. Adolescents reported eating more snacks rather than daily structured meals, and a study of 24-hour diet recall in several countries found increased intake of ultraprocessed foods during the COVID-19 pandemic’s first year.

 Additionally, sleeping patterns were disrupted, and there was an increase in screen time for both school and leisure, especially in low-income families.

 Given these extra stressors and isolation, adolescents reported an increase in “comfort food” consumption, which also contributed to excess weight gain.

Increased weight gain associated with the pandemic has been documented around the world.

 Previously, weight gain trends were known to occur during summer months when children did not have a regular school schedule with structured physical activity and all meals were consumed at home. During the COVID-19 pandemic, similar trends were seen with weight gain when many children were no longer regularly attending school. A disproportionate burden was seen among low-income households.

The COVID-19 pandemic not only exacerbated racial and ethnic disparities present in the United States with higher rates of COVID-19 infection and severe outcomes in Hispanic and non-Hispanic Black children, but it also disproportionally affected food access in these communities.

 Previously, the National School Health Program benefited children of low-income households, allowing access to predictable meals throughout the week. There were attempts to expand the summer lunch program during the COVID-19 pandemic to provide food to families, however, due to a lack of resources, the efforts proved difficult to implement.

Food deserts are areas in low-income neighborhoods with limited food resources, particularly for healthy and fresh foods such as fruits, vegetables, and whole grains. There is a larger presence of fast-food restaurants and convenience stores offering predominantly ultraprocessed foods.

 Food insecurity is defined as limited or uncertain access to food that is nutritionally adequate due to lack of money or ways to acquire food.

 Households with less financial stability and fewer resources often are those with higher rates of obesity.

 Children living in poverty also are experiencing higher rates of infection and severe disease during the COVID-19 pandemic.

During the COVID-19 pandemic, food insecurity increased and families purchased ultraprocessed foods more often due to lower cost and the foods’ longer shelf life.

 Decisions about the most cost-effective methods to provide food were influenced by lower costs for higher-calorie foods.

 During lockdown with social distancing, acquiring foods became even more difficult for families with food insecurity, and most families experienced a further reduction in income, only exacerbating the problem.

 Food insecurity rates in families tripled 6 weeks after the lockdown and overall food insecurity rates increased by approximately 20% in the United States and contributed to poor quality of diet.

 Children are often aware of their family’s food insecurity despite parental attempts to shelter them of that fact.

For clinicians, engaging with both parents and adolescents during visits creates an environment of shared decision-making, and motivational interviewing can lead to the most success for implementing dietary changes. Potential engaging questions that lead to action are included in Table 2. Utilizing a multidisciplinary approach, including access to behavioral psychologists and dietitians to help with decision-making and meal planning, also can be helpful.

Screening for social determinants of health with a focus on food security is becoming a common practice in pediatrician offices due to the frequency of visits, even if they are virtual. Whereas education is important, it alone does not have the desired impact on food insecurity. Recognition of social stressors associated with poverty is important due to its disruption of development and contribution to chronic disease. Addressing the “hunger vital sign” to screen for food insecurity can be done at all visits, both in person and virtual.

 Normalization and recognition of the struggle that families face, especially during the COVID-19 pandemic, can help families be more willing to discuss options for assistance.

 Primary care providers should be prepared to discuss social determinants of health in addition to having knowledge about weight concerns and obesity. Providing resources to families and ensuring adequate follow-up are crucial to promote long-term health.

 Active and passive referrals for food resources can be done by providing information for food shelters or giving foods directly to families at the visit.

1. Petrus RR, do Amaral Sobral PJ, Tadini CC, Gonçalves CB. The NOVA classification system: a critical perspective in food science. 

. 2021;116(3):603-608. doi:10.1016/j.tifs.2021.08.010

2. Martínez Steele E, Baraldi LG, da Costa Louzada ML, Moubarac JC, Mozaffarian D, Monteiro CA. Ultra-processed foods and added sugars in the US diet: evidence from a nationally representative cross-sectional study. 

. 2016;6(3):e009892. doi:10.1136/bmjopen-2015-009892

3. Baker P, Machado P, Santos T, et al. Ultra‐processed foods and the nutrition transition: global, regional and national trends, food systems transformations and political economy drivers. 

. 2020;21(12):e13126. doi:10.1111/obr.13126

4. Wang L, Martínez Steele E, Du M, et al. Trends in consumption of ultraprocessed foods among US youths aged 2-19 years, 1999-2018. 

. 2021;326(6):519-530. doi:10.1001/jama.2021.10238

5. Martínez Steele E, Popkin BM, Swinburn B, Monteiro CA. The share of ultra-processed foods and the overall nutritional quality of diets in the US: evidence from a nationally representative cross-sectional study. 

. 2017;15(1):6. doi:10.1186/s12963-017-0119-3

6. Dunford EK, Ng SW, Taillie LS. How does the healthfulness of the US food supply compare to international guidelines for marketing to children and adolescents? 

. 2019;23(6):768-776. doi:10.1007/s10995-018-02693-1

7. Chang K, Khandpur N, Neri D, et al. Association between childhood consumption of ultraprocessed food and adiposity trajectories in the Avon Longitudinal Study of parents and children birth cohort. 

. 2021;175(9):e211573. doi:10.1001/jamapediatrics.2021.1573

8. Calcaterra V, Vandoni M, Pellino VC, Cena H. Special attention to diet and physical activity in children and adolescents with obesity during the coronavirus disease-2019 pandemic. 

. 2020;8:407. doi:10.3389/fped.2020.00407

9. Neri D, Martinez‐Steele E, Monteiro CA, Levy RB. Consumption of ultra‐processed foods and its association with added sugar content in the diets of US children, NHANES 2009‐2014. 

. 2019;14(12):e12563. doi:10.1111/ijpo.12563

10. Lane MM, Davis JA, Beattie S, et al. Ultraprocessed food and chronic noncommunicable diseases: a systematic review and meta‐analysis of 43 observational studies. 

. 2021;22(3):e13146. doi:10.1111/obr.13146

11. Barco Leme AC, Fisberg RM, Baranowski T, et al. Perceptions about health, nutrition knowledge, and MyPlate food categorization among US adolescents: a qualitative study. 

. 2021;53(2):110-119. doi:10.1016/j.jneb.2020.11.008

12. Dunford EK, Ng SW, Taillie LS. How does the healthfulness of the US food supply compare to international guidelines for marketing to children and adolescents? 

. 2019;23(6):768-776. doi:10.1007/s10995-018-02693-1

13. Tester JM, Rosas LG, Leung CW. Food insecurity and pediatric obesity: a double whammy in the era of COVID-19. 

 2020;9(4):442-450. doi:10.1007/s13679-020-00413-x

14. Adams EL, Caccavale LJ, Smith D, Bean MK. Food insecurity, the home food environment, and parent feeding practices in the era of Covid‐19. 

. 2020;28(11):2056-2063. doi:10.1002/oby.22996

15. Lange SJ, Kompaniyets L, Freedman DS, et al. Longitudinal trends in body mass index before and during the COVID-19 pandemic among persons aged 2-19 years -United States, 2018-2020. 

. 2021;70(37):1278-1283. doi:10.15585/mmwr.mm7037a3

16. Teixeira MT, Vitorino RS, da Silva JH, Raposo LM, de Aquino LA, Ribas SA. Eating habits of children and adolescents during the COVID‐19 pandemic: the impact of social isolation. 

. 2021;34(4):670-678. doi:10.1111/jhn.12901

17. White A, Liburd LC, Coronado F. Addressing racial and ethnic disparities in COVID-19 among school-aged children: are we doing enough? 

. 2021;18:E55. doi:10.5888/pcd18.210084


Articles

Disruptions to routines and economic troubles have affected the diets of families. Here’s how to foster better nutrition.

Eating habits of children during COVID-19

Infants who have a history of intestinal injury as neonates can pose challenges for the pediatricians who care for these babies after they are discharged from the hospital. Here are some of the causes, feeding guidelines, and approaches to feeding difficulties that you can use in your practice.

Common causes of neonatal intestinal injury include necrotizing enterocolitis (NEC), spontaneous intestinal perforation, gastroschisis, intestinal atresia, and volvulus (Table 1). Intestinal injury in the neonate typically presents acutely with vomiting, inability to tolerate enteral feeds, abdominal distention, and bloody stools. Treatment typically requires at least the temporary adoption of bowel rest and parenteral nutrition.

Intestinal failure is generally defined by the loss of normal function of the intestine, regardless of length of residual small bowel, resulting in reliance on parenteral nutrition for calories and fluid to sustain life. NEC and gastroschisis are the most common causes of long-term intestinal failure in infants, which results in significant morbidity, mortality, and cost to families and medical systems.

 Those infants who undergo significant intestinal resection and intestinal failure, and thus need long-term parenteral nutrition, require specialized care in multidisciplinary intestinal rehabilitation centers. However, the majority of infants with intestinal injury will tolerate enteral nutrition by hospital discharge.

 Therefore, the majority of these infants will be cared for by their primary pediatricians, who should be aware that these infants are prone to a variety of ongoing nutritional challenges.

Feeding difficulties include poor oral intake, failure to thrive, nutrient deficiencies, gastroesophageal reflux disease (GERD), and intestinal dysmotility. Intestinal dysmotility secondary to resection or injury can cause chronic vomiting, diarrhea, abdominal distention, and small intestinal bacterial overgrowth (SIBO). More than 50% of infants with intestinal injury are prescribed medications to address 1 or more of these issues.

 Overall positive prognostic indicators for successful tolerance of enteral feeds in these infants include the residual length of the small bowel following resection (the longer the residual bowel, the better), the presence of an intact ileocecal valve, and an intact colon; therefore, it is important to understand the infant’s surgical course, residual anatomy, and any neurodevelopmental sequelae.

General feeding guidelines and principles

The importance of feeding guidelines and algorithms for preterm and other critically ill infants who are at increased risk of NEC are well established.

 However, guidelines for feeding following intestinal injury are not standardized; they can be highly variable across institutions and even among providers at the same institutions.

Enteral feeding stimulates the intestine to heal and grow. Data have shown that early implementation of enteral feeds following intestinal injury (<5-7 days) promotes intestinal adaptation and is not associated with worse outcomes

 or recurrence of NEC. In fact, early feeding with the use of consistent, standardized feeding advancement has been associated with shorter length of stay, quicker achievement of enteral feeding goals, fewer infectious complications, and reduced overall cost to the patient and health system.

 For those patients who require surgery for intestinal injury, guidelines support early post-operative enteral feeding with breast milk if available.

Once infants are advanced to full enteral feeds, close monitoring of weight is needed to ensure age-appropriate weight gain. A follow-up study of infants with intestinal injury demonstrated that a majority of these infants will be discharged with some proportion of supplemental tube feeding via nasogastric or gastrostomy tube, but most will be weaned to primarily oral feeds by the time they are aged 1 year.

 Those with a history of NEC and spontaneous intestinal perforation were found to have poor weight gain 3 months after discharge.

 In some studies, poor weight gain in children with surgical NEC persisted through the first 2 years of life.

 Infants with intestinal injury therefore require frequent feeding adjustment and weight checks in those early months to account for higher caloric requirements for optimal growth. Foods that are complementary to formula and breast milk should be added to the diet as developmentally appropriate, with the provision that fruit juices and sugary foods can produce a high solute load in the small bowel. Children with intestinal dysfunction or resection may be more prone to the osmotic diarrhea caused by these foods.

Breast milk has long been favored as the initial choice for feeding infants both with and without intestinal injury or resection. Breast milk reduces the risk of NEC. Breast milk attenuates the proinflammatory pathway that is mediated by a molecular signaling protein, Toll-like receptor-4, which plays a prominent role in the pathogenesis of NEC.

 The exclusive use of preterm formula instead of breast milk might contribute to maturation of less-favorable intestinal flora, and it lacks the protective effects against NEC that are seen in preterm infants who are fed breast milk. If maternal breast milk is not available to infants with intestinal injury, donor breast milk should be used, if available. Donor milk has also been shown to be protective against further intestinal injury, despite the need for pasteurization.

Breast milk also has a multitude of beneficial bioactive and immunomodulating components that not only provide nutrition but also provide anti-inflammatory and antioxidant compounds.

 Examples include epidermal growth factors, which promote mucosal healing; secretory immunoglobulin A for immune function; lactoferrin to promote enterocyte growth; and prebiotic substrates, such as human milk oligosaccharides (HMOs), which promote a diverse gut flora. HMOs are carbohydrates found in human milk; they have antimicrobial properties that prevent the adhesion of some pathogenic intestinal bacteria. HMOs diminish intestinal leukocyte adhesion and migration, thereby dampening some of the pro- inflammatory processes in the gut. Synthetically produced HMOs are now available, but not all are functionally equivalent to endogenously produced HMOs.

Despite breast milk’s many benefits, not all infants with intestinal injury will have access to it or will tolerate it. Formula selection should take into consideration the degree of intestinal injury and other comorbidities. A list of infant formulas and their properties is shown in Table 2. Among infants who had significant bowel injury requiring parenteral nutrition, those who were fed amino acid–based formula, also known as elemental formula, or breast milk required parenteral nutrition for a shorter duration, indicating that amino acid–based formula was also well tolerated by such infants.

 The amino acids and medium-chain triglycerides in these formulas are simpler to absorb.

Extensively hydrolyzed formulas should be considered in patients who have suspected milk protein intolerance. Infants who are born extremely prematurely and/or who are critically ill have been found to have worse outcomes with the use of intact-protein, cow’s milk–based formulas.

 These formulas are associated with developing NEC, which can be recurrent; therefore, they should be used cautiously in infants with a NEC history. The elemental formulas (amino-acid based) may be better tolerated; however, more complex intact proteins and other macronutrients promote a greater degree of intestinal growth and adaptation after intestinal resection. Intact cow’s milk proteins may be tolerated later in those infants with more significant bowel injury or resection as the infant’s immune system matures. Term infants with minimal resection may tolerate an intact cow’s milk–based formula initially following intestinal injury.

Even if they are successfully weaned from parenteral nutrition, infants with bowel injury may still be prone to feeding difficulty due to anatomic changes, dysmotility, and developmental delay. Nearly 60% of infants who experience NEC will have neurodevelopmental delay, which can have a negative impact on their ability to feed orally.

 Common symptoms of feeding intolerance include oral aversion, vomiting, fussiness with feeding, abdominal distention, and change in stool frequency and consistency. Treatment and evaluation should be tailored to the infant’s symptoms and medical history.

Certain infants—those with a history of neurodevelopmental delay or who required prolonged periods of bowel rest and parenteral nutrition early in life—may experience poor development of oral-motor coordination or oral aversion. Clinical signs of this include dysphagia, gagging with feeds, or oral feed refusal. Such children might require swallow evaluation with a speech-language pathologist and referral for feeding therapies with a multidisciplinary feeding rehabilitation program.

 Clinical reflux is also a common cause of vomiting and fussiness with feeds. However, the possibilities of delayed gastric emptying or partial obstruction also need consideration, particularly in infants with a history of NEC, gastroschisis, or intestinal reanastomosis; all are prone to dysmotility and strictures.

Radiographic studies can aid in the diagnostic evaluation of anatomic etiologies. They can include (1) abdominal x-ray, to assess for evidence of bowel obstruction or ileus; (2) contrast upper gastrointestinal series or contrast enema to evaluate for stricture, dilatation, or malrotation; and (3) abdominal ultrasound to evaluate both the intestines (intussusception, stricture, or gastric outlet obstruction) and surrounding organs (hydronephrosis).

If no structural cause for vomiting is identified, medications and feeding changes may be indicated. Empiric treatment with 4 to 8 weeks of histamine-2 blockers, proton pump inhibitors (PPIs), or pro-motility agents such as erythromycin can be trialed for suspected reflux. Potential feeding interventions include providing a smaller volume of food with each feeding, more frequent feedings, transitioning to an extensively hydrolyzed or amino acid–based formula, or, ultimately, continuous feeding via nasogastric or gastrostomy tube if other measures fail. Some infants may also require enteral tube feeding due to dysphagia or severe oral aversion. Management of ongoing enteral tube feeding or poor response to formula or medication changes warrants referral to a pediatric dietician and gastroenterologist.

Infants with a history of intestinal injury or bowel resection who experience abdominal distention or bloating without obstruction, feeding intolerance, and changes in stool patterns may have SIBO. Factors that predispose an infant to SIBO include anatomic intestinal abnormalities, dysmotility, bowel resection, ileocecal valve resection, and prolonged use of PPIs that alter the gut flora. In severe cases, SIBO can cause malabsorption, severe diarrhea, acidosis, and altered mental status.

The diagnosis of SIBO can be challenging, as the gold-standard diagnosis technique requires bacterial quantification of jejunal secretions via endoscopy or hydrogen breath testing, neither of which is easily obtained in infants or young children.

 Therefore, empiric treatment with antibiotics is often trialed if there is a strong clinical suspicion of SIBO. A variety of SIBO treatment regimens in children have been proposed (Table 3); however, there is no consensus guideline for pediatric regimens. Empiric treatment is typically prescribed for a 7- to 10-day course, with some infants requiring long-term cycled antibiotics: alternating 1 or 2 antibiotics every 2 to 4 weeks in an effort to prevent development of bacterial resistance. The antibiotic doses for SIBO are typically lower than those in traditional regimens for treating infection, as the goal is to overall reduce the gut bacterial flora.

There has been great interest in the use of probiotics and prebiotics in infants in recent years. Probiotics are live microorganisms that are administered as an oral supplement to help maintain the balance of beneficial gut bacteria and gut health. Prebiotics are nondigestible oral supplements, usually made up of oligosaccharides, that serve as substrates for nonpathogenic gut bacteria.

 The positive balance of pathogenic and nonpathogenic intestinal microorganisms has an effect on underlying gut inflammation and health.

Preterm infants have later acquisition of and fewer beneficial gut bacteria, including 

, when compared with term infants. This lack of diversity is multifactorial and related to mode of delivery, exposure to antibiotics, the hospital environment, and feeding methods.

 The use of probiotics and prebiotics has served to promote and maintain the balance of nonpathogenic gut bacteria, with some data indicating benefits of certain probiotic strains including 

Recent American Gastroenterological Association guidelines recommend the use of probiotics in preterm and low-birth-weight infants that contain a combination of 

 However, the benefit of probiotics in infants following intestinal injury is unclear and, currently, insufficient evidence recommends the routine use of probiotics following intestinal injury.

 There is no consensus regarding the optimal dose or frequency of probiotics or prebiotics in children, and it is important to note that there have been case reports of bacterial translocation and bacteremia associated with probiotic use in infants.

 Although probiotics and prebiotics have shown promising beneficial effects in some pediatric patients, their use should be deter- mined on a case-by-case basis in lower-risk infants.

Even those infants with relatively short segments of bowel resection should be monitored for nutrient deficiencies. Risk is related to the particular location of resected bowel and the degree of dysmotility causing diarrhea with malabsorption. For example, copper is absorbed primarily in the proximal small intestine, so resections or dysfunction of the duodenum and proximal jejunum can lead to copper deficiency. Vitamin B

 is absorbed only in the terminal ileum, and B

 deficiency may not become apparent for several months after resection of the terminal ileum. Additional common nutrient deficiencies to be aware of include iron-deficiency anemia, copper-deficiency anemia, and deficiencies of fat-soluble vitamins (A, D, E, K) and of trace minerals such as selenium and zinc (Table 4).

 Depending on clinical signs and symptoms, and on the infant’s pattern of bowel injury, these levels should be monitored 1 to 2 times per year for the first 2 to 3 years, or more frequently if repletion is needed.

Infants with a history of intestinal in- jury from neonatal conditions such as NEC, gastroschisis, and other etiologies of intestinal resection are predisposed to feeding difficulties and nutritional deficiencies. The infant’s surgical history and remaining bowel anatomy need to be considered when monitoring feeding tolerance, growth, and nutritional status. These infants often require the use of hydrolysate or elemental formula if breast milk is not tolerated; however, the use of breast milk should be prioritized given its unique immunologic and probiotic benefits. Feeding intolerance, poor growth, GERD, and dysmotility can also be managed with feeding volume and rate adjustments, and with the assistance of various medications if anatomic etiologies, such as stricture, have been excluded.

1. Neu J, Walker WA. Necrotizing enterocolitis. 

 2011;364(3):255-264. doi:10.1056/NEJMra1005408

2. Squires RH, Duggan C, Teitelbaum DH, et al. Pediatric Intestinal Failure Consortium. Natural history of pediatric intestinal failure: initial report from the Pediatric Intestinal Failure Consortium. 

 2012;161(4):723-728.e2. doi:10.1016/j.jpeds.2012.03.062

3. Jones IH, Hall NJ. Contemporary outcomes for infants with necrotizing enterocolitis–a systematic review. 

 2020;220:86-92.e3. doi:10.1016/j.jpeds.2019.11.011

4. Belza C, Fitzgerald K, de Silva N, et al. Predicting intestinal adaptation in pediatric intestinal failure: a retrospective cohort study

 2019;269(5):988-993. doi:10.1097/SLA.0000000000002602

5. Wales PW, Allen N, Worthington P, George D, Compher C, American Society for Parenteral and Enteral Nutrition, Teitelbaum D. A.S.P.E.N. clinical guidelines: support of pediatric patients with intestinal failure at risk of parenteral nutrition-associated liver disease. 

 2014;38(5):538-557. doi:10.1177/0148607114527772

6. Xu JH, Coo H, Fucile S, et al; Canadian Neonatal Network Investigators. A national survey of the enteral feeding practices in Canadian neonatal intensive care units. 

 2019;25(8):529-533. doi:10.1093/pch/pxz112

7. Moschino L, Duci M, Fascetti Leon F, et al. Optimizing nutritional strategies to prevent necrotizing enterocolitis and growth failure after bowel resection. 

8. Shores DR, Mogul D, Allen J, Delarmente BA, Padula W. Cost-effectiveness analysis of feeding guidelines for infants following intestinal surgery. 

 2020;70(5):657-663. doi:10.1097/MPG.0000000000002642

9. Shakeel F, Newkirk M, Sellers A, Shores DR. Postoperative feeding guidelines improve outcomes in surgical infants. 

 2020;44(6):1047-1056. doi:10.1002/jpen.1726

10. Varma S, Bartlett EL, Nam L, Shores DR. Use of breast milk and other feeding practices following gastrointestinal surgery in infants. 

 2019;68(2):264-271. doi:10.1097/MPG.0000000000002128

11. Hintz SR, Kendrick DE, Stoll BJ, et al; NICHD Neonatal Research Network. Neurodevelopmental and growth outcomes of extremely low birth weight infants after necrotizing enterocolitis. 

 2005;115(3):696-703. doi:10.1542/peds.2004-0569

12. Good M, Sodhi CP, Egan CE, et al. Breast milk protects against the development of necrotizing enterocolitis through inhibition of Toll-like receptor 4 in the intestinal epithelium via activation of the epidermal growth factor receptor. 

 2015;8(5):1166-1179. doi:10.1038/mi.2015.30

13. Hodzic Z, Bolock AM, Good M. The role of mucosal immunity in the pathogenesis of necrotizing enterocolitis. 

14. Bode L, Jantscher-Krenn E. Structure-function relationships of human milk oligosaccharides. 

 2012;3(3):383S-391S. doi:10.3945/an.111.001404

15. Andorsky DJ, Lund DP, Lillehei CW, et al. Nutritional and other postoperative management of neonates with short bowel syndrome correlates with clinical outcomes. 

 2001;139(1):27-33. doi:10.1067/mpd.2001.114481

16. Abrams SA, Schanler RJ, Lee ML, Rechtman DJ. Greater mortality and morbidity in extremely preterm infants fed a diet containing cow milk protein products. 

 2014;9(6):281-285. doi:10.1089/bfm.2014.0024

17. Kerzner B, Milano K, MacLean WC Jr, Berall G, Stuart S, Chatoor I. A practical approach to classifying and managing feeding difficulties. 

 2015;135(2):344-353. doi:10.1542/peds.2014-1630

18. Malik BA, Xie YY, Wine E, Huynh HQ. Diagnosis and pharmacological management of small intestinal bacterial overgrowth in children with intestinal failure. 

 2011;25(1):41-45. doi:10.1155/2011/604643

19. Mangal Patel R, Wei Denning P. Therapeutic use of prebiotics, probiotics, and postbiotics to prevent necrotizing enterocolitis: what is the current evidence? 

 2013;40(1):11-25. doi:10.1016/j.clp.2012.12.002

20. Preidis GA, Weizman AV, Kashyap PC, Morgan RL. AGA technical review on the role of probiotics in the management of gastrointestinal disorders

 2020;159(2):708-738.e4. doi:10.1053/j.gastro.2020.05.060

21. Fallon EM, Nehra D, Potemkin AK, et al. American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.) Board of Directors, Puder M. A.S.P.E.N. clinical guidelines: nutrition support of neonatal patients at risk for necrotizing enterocolitis. 

 2012;36(5):506-523. doi:10.1177/0148607112449651

22. Bertelli C, Pillonel T, Torregrossa A, et al. Bifidobacterium longum bacteremia in preterm infants receiving probiotics. 

 2015;60(6):924-927. doi:10.1093/cid/ciu946.

23. Diab L, Krebs NF. Vitamin excess and deficiency. 

 2018;39(4):161-179. doi:10.1542/pir.2016-0068

24. Bielawska B, Allard JP. Parenteral nutrition and intestinal failure. 

25. Vandenplas Y, Bhatia J, Shamir R, et al. Hydrolysed formulas for allergy prevention. 

. 2014;58(5):549-552. doi:10.1097/MPG.0000000000000318

A history of intestinal injury can create some feeding challenges for infants. Here are some of the causes, feeding guidelines, and approaches to feeding difficulties to use in practice.

Neonatal feeding in practice: Nutrition principles for babies with a history of intestinal injury or resection

Cystic fibrosis (CF) is the most common lethal autosomal recessive disease in the United States, occurring in 2000 to 4000 newborns.

 It is caused by one of the more than 2000 mutations of the CF transmembrane conductance regulator (CFTR). Although most of its morbidity and mortality stems from pulmonary decline, it was first recognized in 1938 as a cause of severe failure to thrive in infants due to characteristic pancreatic insufficiency. Decades later, we are starting to understand the full implication of the effects CFTR mutations on the entirety of the gastrointestinal (GI) system (Table 1).

The CFTR transports chloride and bicarbonate across the apical surface of epithelial cells in the respiratory and GI tracts. Mutations are classified as I to VI, with I to III being the most severe. Mutations result in abnormal structure, synthesis, and/or function of the CFTR protein.

Newborn screening detects trypsinogen, a protein released from the pancreas during the process of its destruction in utero. However, there are false negative results or cases where the specimen is unacceptable, or not received, and there is no appropriate follow-up. As 60% of infants are born with pancreatic insufficiency and another 30% will develop insufficiency in the next 3 years, and as GI, pancreatic, and hepatic manifestations are the most common initial manifestations of CF, before pulmonary manifestations become apparent, clinicians should have a low threshold for obtaining additional testing if CF is suspected.

Achieving optimal growth in early life correlates with fewer pulmonary exacerbations and fewer hospitalizations.

 Infants with CF should be seen monthly to monitor proper growth and then every 3 months for routine care.

 Patients with suboptimal growth should be seen more frequently.

Children with CF require 110% to 200% of normal caloric intake to achieve normal growth.

 In general, the goal body mass index (BMI) is the 50th percentile for age, or the 50th percentile weight-for-length in children aged younger than 2 years. In instances where BMI offers a poor reflection of nutritional status, such as hepatomegaly or ascites, mid-arm circumference serves as an alternative measure. Attainment of nutritional goals involves adequate caloric intake, supplementation with fat-soluble vitamins (A, D, E, K), and pancreatic enzyme replacement therapy (PERT) under the guidance of a CF-trained nutritionist.

In addition to BMI, stunted height must be screened for, as height also correlates with lung function.

 There are multiple causes of stunting in CF (Table 2). A chronic inflammatory state makes insulin-like growth factor 1 (IGF1) less responsive to growth hormone. In addition, CF-related diabetes (CFRD), a unique form of diabetes specific to CF, can lead to growth failure.

Zinc deficiency from malabsorption and sodium deficiency related to CFTR dysfunction also can contribute to poor growth.

 Serum sodium may be normal despite depleted body sodium. A urine sodium to creatinine ratio can be measured. Cystic Fibrosis Foundation (CFF) guidelines emphasize sodium supplementation from infancy onward and with exercise. Zinc supplementation can be instituted empirically if a child is failing to thrive.

Due to fat malabsorption and dysregulation of fatty acid metabolism, patients with CF frequently have essential fatty acid deficiency (EFAD),

 which contributes to poor growth and can lead to immune system compromise, dermatitis, alopecia, and thrombocytopenia.

In young children, picky eating can lead to inadequate weight gain. Although often a behavioral issue, underlying pathology from eosinophilic or celiac disease can manifest as picky eating, so these should be considered. All patients and families should be screened for food insecurity.

Attainment of nutritional goals is important. If a child is failing to meet goals, early discussions around invasive interventions such as nasogastric, gastrostomy, gastrojejunal, or jejunal tubes should be undertaken, as families may need time to become comfortable with these ideas.

Sixty percent of newborns with CF are born with complete pancreatic insufficiency (PI), and another 25% develop it by age 1 year.

 A baseline fecal elastase should be obtained in the neonatal period to assess for pancreatic sufficiency. Patients can develop PI at any time without early symptoms to indicate change. Annual monitoring with fecal elastase is recommended. A decrease in fecal elastase precedes steatorrhea. Steatorrhea develops only after lipase output falls below 10%. Fecal elastase can be falsely positive in watery stool and in severe nutritional depletion. In the latter case, testing should be repeated once nutritional repletion is addressed.

Pancreatic enzyme replacement therapy is critical to nutrient absorption and growth. It is important to optimize the timing of enzymes when the child is actively eating or immediately after, not prior to meals. Schools may need additional information about proper medication timing.

DYSMOTILITY: MECONIUM IIEUS (MI), INTUSSUSCEPTION, CONSTIPATION, AND DISTAL INTESTINAL OBSTRUCTION SYNDROME (DIOS)

Children with CF have an altered intraluminal intestinal environment. Gut microbiome changes in CF are already detected at 15 days of life.

 Breastfeeding can help promote diversity but does not eliminate all the issues related to CFTR dysfunction. This CFTR dysfunction leads to a dehydrated intestinal mucin layer and inspissated secretions. Decreased pancreatic bicarbonate secretion changes pH, and together with overexposure to acid reducers and antibiotics results in altered gut microbiota with diminished diversity, which can mimic a Crohn-like microbiome.

 The diminished diversity can lead to overgrowth of bacteria, impairing the enteric nervous system and contributing to slowed motility and stagnation.

In the neonatal period this manifests as meconium ileus (MI), occurring in up to 25% of neonates with CF.

Significant improvements in cystic fibrosis (CF) care have focused primarily on the pulmonary system, but addressing the gastrointestinal complications of CF presents a major opportunity for improvement in disease management.

Darla Shores, MD, PhD

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Neonatal feeding in practice: Nutrition principles for babies with a history of intestinal injury or resection

Gastrointestinal manifestations of cystic fibrosis: A primer for pediatricians