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Optimizing Care and Outcome for Late-Preterm (Near-Term) Infants: A Summary of the Workshop Sponsored by the National Institute of Child Health and Human Development

^a National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland
^b Division of Neonatology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
^c Department of Obstetrics and Gynecology, University of Texas Southwestern Medical Center, Dallas, Texas

	ABSTRACT

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

 
In 2003, 12.3% of births in the United States were preterm (<37 completed weeks of gestation). This represents a 31% increase in the preterm birth rate since 1981. The largest contribution to this increase was from births between 34 and 36 completed weeks of gestation (often called the "near term" but referred to as "late preterm" in this article). Compared with term infants, late-preterm infants have higher frequencies of respiratory distress, temperature instability, hypoglycemia, kernicterus, apnea, seizures, and feeding problems, as well as higher rates of rehospitalization. However, the magnitude of these morbidities at the national level and their public health impact have not been well studied. To address these issues, the National Institute of Child Health and Human Development of the National Institutes of Health invited a multidisciplinary team of experts to a workshop in July 2005 entitled "Optimizing Care and Outcome of the Near-Term Pregnancy and the Near-Term Newborn Infant." The participants discussed the definition and terminology, epidemiology, etiology, biology of maturation, clinical care, surveillance, and public health aspects of late-preterm infants. Knowledge gaps were identified, and research priorities were listed. This article provides a summary of the meeting.

Key Words: prematurity • low birth weight • preterm birth • near-term infant • late-preterm infant • seizures • kernicterus • respiratory distress syndrome • apnea • sudden infant death

Abbreviations: TTN—transient tachypnea of the newborn • RDS—respiratory distress syndrome

The rate of preterm births in the United States increased from 9.1% in 1981 to 12.3% in 2003,¹ an increase of 31%, most of which was caused by increases in the proportion of so called near-term births, referred to as "late preterm" in this article. The obstetric and neonatal care at late-preterm gestations presents many challenges to the health care team. The obstetrician has to weigh the risks and benefits of immediate delivery versus expectant management of the pregnant patient. The pediatrician has the task of caring for a preterm infant who may be seemingly healthy but is at higher risks than term infants for several neonatal morbidities,^2–7 higher rates for readmissions,^7–10 and higher neonatal and postneonatal mortality rates.^{11, 12}

Although some studies have addressed these issues, there is no unanimity about the magnitude of these problems, even among experts. Moreover, nationwide data are not available to assess the collective impact of late-preterm births on the overall health care system. To address these issues, the National Institute of Child Health and Human Development of the National Institutes of Health invited a group of experts (listed in "Acknowledgments") to a workshop in July 2005. This article provides a summary of the proceedings. Individual presentations from the workshop are published in 2 special issues of Seminars in Perinatology (2006, volume 30, number 1, February, and number 2, April).

	DEFINITIONS AND TERMINOLOGIES

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

 
The American Academy of Pediatrics and the American College of Obstetricians and Gynecologists define a "preterm" infant as one who is born before the end of the 37th week (259th day) of pregnancy, counting from the first day of the last menstrual period.¹³ However, there is no consensus on the definition of "near term." Besides a wide range of gestational-age combinations between 33 weeks and term, descriptive terms such as "marginally preterm," "moderately preterm," "minimally preterm," and "mildly preterm" have been used to describe this subset of preterm infants.

The panel suggested to consider designating infants born between the gestational ages of 34 weeks and 0/7 days through 36 weeks and 6/7 days (239th–259th day) as "late preterm" and discontinue the use of the phrase "near term." The panel was of the opinion that "near term" can be misleading, conveying an impression that these infants are "almost term," resulting in underestimation of risk and less-diligent evaluation, monitoring, and follow-up. The panel confirmed that gestational age should be rounded off to the nearest completed week, not to the following week.¹⁴ Thus, an infant born on the 5th day of the 36th week (35 weeks and 5/7 days) is at a gestational age of 35 weeks, not 36 weeks.

Several factors were considered in recommending the gestational age range of 34 0/6 to 36 6/7 weeks to define late preterm. In obstetric practice, 34 completed weeks is considered a maturational milestone for the fetus.¹⁵ Yet, compared with term infants, those born between the 34th and 37th week of gestation suffer from higher rates of morbidity and mortality.^2–12 Because there is no such thing as a normal preterm infant, "late preterm" conveyed the sense of vulnerability of these infants better than did the phrase "near term." The panel noted that maturation is a continuous process, and any classification is bound to be arbitrary. However, the panel underscored the value of a uniform definition and suggested additional research on this topic:

• Develop a risk-based system to subclassify the heterogeneous category of preterm infants to improve the precision of risk assessment and comparability of outcomes.
  
• Refine methods to assess pregnancy duration and fetal/neonatal gestational ages and maturity.
  
• Develop gestational-age–specific anthropometric indices for singleton and multiple gestations among different ethnic groups to classify infants into appropriate risk categories.
  
• Educate physicians, nurses, and other health care personnel that even seemingly healthy, late-preterm infants (formerly known as near-term infants) are to be considered physiologically immature and should be diligently evaluated, monitored, and followed.
  

	EPIDEMIOLOGY

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

 
Using the US data for 1992 and 2002, Davidoff et al¹⁶ found that two thirds of the decade's increase in preterm births was caused by an increase in the rate of late-preterm births. Also noteworthy was that 74.1% of all singleton preterm births in 2002 occurred at 34, 35, and 36 weeks of gestation (342234 of 394996 singleton preterm births).¹⁶ Because they constitute such a large proportion of preterm infants, even a modest increase in their birth rate can have a huge impact on health care cost. For example, compared with 1992, in 2002 there was an increase of 1.3% in singleton late-preterm births, resulting in a net increase of 45589 preterm infants.¹⁶ Although there have been studies that described the trends in preterm births in the United States,¹⁷ there were no large-scale prospective studies that explored the etiology of late-preterm births or assessed their impact on the national health care system. The panel suggested additional areas for research on this topic:

• Describe the epidemiology of late-preterm births in different ethnic and sociodemographic subgroups in the United States.
  
• Use the national data to examine the etiology of late-preterm births and assess their proportion resulting from established indications and those that are possibly preventable. Stratify the analyses according to the place of infant birth, mother's payer status, and level of hospital care where the infant is delivered.
  
• Assess the contribution of the gestational-age–specific preterm birth rate to overall neonatal and infant mortality and morbidity. Describe and assess the cause-specific and gestational-age–specific morbidity and mortality for late-preterm births in the US population.
  
• Measure the economic impact of the high late-preterm birth rates on the initial and later hospitalization costs, and on the long-term health effects that require early intervention and other medical and social services.
  
• Evaluate postdischarge outcomes and morbidity for late-preterm infants, categorizing them according to the levels of hospital care and payer status and focusing on the identification of risk factors for readmissions.
  

	OBSTETRICAL ISSUES

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

 
The management of women in labor at any preterm gestation presents many challenges for the obstetrician.^18–21 The best time to deliver has to be based on the anticipated risks to the mother and the fetus from expectant management versus the risks and benefits to the mother and the newborn of early delivery. Although being born prematurely increases neonatal morbidity and mortality, expectant management of the pregnancy when the fetus is in a potentially hostile intrauterine environment can lead to fetal compromise. This may increase the risks for fetal and neonatal organ dysfunctions, including neurologic injury or fetal or neonatal death.

Although the factors contributing to increasing preterm births in the United States remain to be identified, plausible etiologies include increasing proportion of pregnant women >35 years of age, multiple births, medically indicated deliveries secondary to better surveillance of the mother and the fetus, attempts to reduce stillbirths, and stress from a variety of sources.^18–21 Some well-known medically indicated factors leading to late-preterm births include placental abruption, placenta previa, bleeding, infection, hypertension, preeclampsia, idiopathic preterm labor, premature rupture of membranes, intrauterine growth restriction, and multiple gestation. Using a population-based data set for 1996, Gilbert et al,²² however, concluded that avoiding "non-medically indicated births" between 34 and 37 weeks of gestation could have saved $49.9 million in California. But, the panel observed that more research is needed not only to validate the Gilbert et al data but also to refine management of the fetus and the mother at late-preterm gestation:

• Develop evidence-based data to assess risk/benefit ratios for diagnosis-specific indications for delivery at late-preterm gestations.
  
• Evaluate strategies to improve specific outcomes in late-preterm infants. One such strategy may be to study the effect of antenatal steroids in enhancing pulmonary maturity in the late-preterm fetus, especially in multiple gestations.²³
  
• Study ways to improve the precision of estimates of pregnancy duration, possibly by implementation of routine first-trimester ultrasound for dating, which has shown to improve the accuracy to within 5 days compared with other dating methods.
  
• Study the factors associated with accelerated and delayed fetal organ maturation, because gestational age and organ maturation may not be linearly related.
  
• Improve the accuracy of estimating fetal well-being in the presence of maternal diseases (eg, hypertension, diabetes, prolonged rupture of membranes, and chorioamnionitis) to plan for appropriate time and route of delivery.
  
• Develop strategies to identify a fetus at risk for late-pregnancy intrauterine death.
  
• Study the effects of physician/obstetrician availability, on-call patterns, and insurance policies on obstetric practices related to late-preterm births.
  

	NEONATAL ISSUES

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

 
Temperature Instability and Hypoglycemia
Late-preterm infants are at risk for hypothermia and early hypoglycemia as a result of immaturity and a failure to transition adequately between intrauterine and extrauterine life during the first 12 hours of age.^{24, 25} Hypothermia and hypoglycemia can potentially worsen preexistent respiratory distress.

Cardiopulmonary System
Transient tachypnea of the newborn (TTN) and respiratory distress syndrome (RDS) in late-term infants have been well studied.^{7, 23, 26–30} Lack of clearance of lung fluid and/or relative deficiency of pulmonary surfactant, respectively, remain central to the pathophysiology of these disorders, and birth in the absence of labor and related hormonal changes also contribute to pulmonary dysfunction.²³ However, stricter criteria are needed to define and distinguish TTN, RDS, and pneumonia.

Few studies have evaluated the frequency of apnea of prematurity and its treatment in the late-preterm infant. Late-preterm infants are at a twofold higher risk for sudden infant death syndrome (1.4 cases per 1000 at 33–36 weeks' gestation, compared with 0.7 per 1000 at >37 weeks' gestation), although the mechanisms are not known.^{12, 31–34}

Gastrointestinal Tract
The gastrointestinal tract continues to develop throughout gestation, but late-preterm infants adapt quickly to enteral feedings, including the digestion and absorption of lactose, proteins, and lipids.^35–37 However, deglutition and peristaltic functions and the sphincter controls in the esophagus, stomach, and intestines are likely be less mature in late-preterm infants compared with term infants,³⁷ which may lead to difficulty in coordinating suck and swallowing, a delay in successful breastfeeding, poor weight gain, and dehydration during early postnatal weeks.^8–10 Changes in the ecology of gastrointestinal bacteria in the relatively immature gut of the late-preterm infant, and their potential impact on growth and later health (allergy, diabetes), remain to be studied.^{38, 39}

Brain
Late-preterm infants have more immature brains compared with term infants; it is estimated that at 35 weeks of gestation, the surface of the brain shows significantly fewer sulci, and the weight of the brain is only 60% that of term infants.^{40, 41} Over the final 4 weeks of gestation, dramatic growth is seen in the gyri, sulci, synapses, dendrites, axons, oligodendrocytes, astrocytes, and microglia.^42–47

Hyperbilirubinemia
Late-preterm infants have a higher incidence of prolonged physiologic jaundice and thus remain vulnerable for brain damage from jaundice for longer periods compared with term infants.^{3, 6} If these infants are assumed to be the same as term infants, they may be discharged early with inadequate evaluation of jaundice, and plans for follow-up. Thus, the late-preterm infants may be at higher risk for bilirubin-induced brain injury.⁶

Pharmacology and Drug Therapy
There are very few studies that have described the week-by-week maturation in drug clearance during the final 4 to 6 weeks of gestation. Thus, if one develops dosing guidelines for late-preterm infants that are based on term-infant data, there is a risk for inappropriate drug dosing; immaturity of the liver and kidney in late-preterm infants can reduce drug clearance.⁴⁸ Other factors affecting drug clearance that need to be studied include liver and kidney dysfunctions resulting from disease states and cholestasis associated with parenteral nutrition.

Immunologic System
Compared with term and extremely preterm infants, late-preterm infants are intermediate with regard to immunologic maturity.⁴⁹ However, more studies are needed to understand the temporal trends in maturation of T-cell and granulocyte functions, other immune mediators, and their role in host-defense mechanisms in late-preterm gestations.

Outcome After Initial Hospital Discharge
Despite recommendations by the American Academy of Pediatrics that early postnatal discharge be "limited to infants who are of singleton birth between 38 and 42 weeks' gestation,"⁵⁰ many late-preterm infants are discharged early, often within 48 hours.^7–10 Thus, it is not surprising that their readmission rates are much higher than those for term infants.^7–11 The identified risk factors for readmission include maternal complications during labor and delivery, receiving support from a public payer, Asian/Pacific Islander ethnicity, firstborn infant, and infant being breastfed at discharge.^{1, 7–10} Jaundice, proven or suspected infections, feeding difficulties, and failure to thrive were the most common diagnoses at readmission.⁷

Long-term Outcomes
Few studies have evaluated the long-term neurodevelopmental status of late-preterm infants. Thus, we do not know the prevalence rates for subtle neurologic abnormalities, learning difficulties, poor scholastic achievements, and behavioral problems in infants born at late-preterm gestational ages. In a study of 869 low birth weight infants, Gray et al⁵¹ found that 19% to 20% of the cohort born at 34 to 37 weeks of gestation had clinically significant behavior problems at 8 years of age, a rate higher than those in the term cohorts from the same population.⁵²

Health Care Policy Issues
The polices set by insurance providers often dictate health care practice, such as the site of care (intensive, intermediate, or routine), number and type of tests performed, and the age at discharge. Specific birth weights, rather than gestational age, are often used to determine the length of hospital stay. In some states, infants with birth weights 1500 g are defined as "high risk," implying that the high-risk status for others should be justified on the basis of other criteria, not birth weight or gestational age. However, gestational age, birth weight, the infant being small or large for gestation, and the medical condition should all be used to assess an infant's risk level.

In hospitals in the United States, there is also considerable variation in medical care for newborn infants, especially in the use of mechanical ventilation and nutritional support, despite similar birth weights and admission illness severity.⁵³ Although the reasons for such trends are unknown, variation may lead to increased hospital costs or suboptimal care.

The panel reviewed various neonatal issues related to late-preterm birth (Table 1) and suggested research topics to be considered by the scientific community:

• Conduct studies to assess the risk of TTN, RDS, and severe respiratory failure that may lead to the requirement of such interventions as conventional and high-frequency ventilation, inhaled nitric oxide, and extracorporeal membrane oxygenation support in late-preterm infants.
  
• Identify factors enhancing cardiopulmonary maturity, such as the role of antenatal steroid treatment in reducing TTN and RDS.
  
• Conduct studies to understand the maturation of breathing and deglutition functions in late-preterm infants, which would have implications for apnea of prematurity and feeding.
  
• Conduct studies to document the frequency of later-onset apnea and bradycardia in late-preterm infants and to improve their evaluation and treatment.
  
• Study the risk factors for developmental morbidities and sudden infant death syndrome in late preterm by using large home monitoring data sets that are available, such as the Collaborative Home Infant Monitoring Evaluation.^32–34
  
• Study the nature of vulnerability of the late-preterm infant to white matter injury and evaluate its functional consequences on neurodevelopmental outcomes.
  
• Conduct computed tomography, MRI, and functional MRI studies to understand the ontogeny of brain growth and maturation and to assess the value of routine cranial ultrasound in late-preterm infants in helping to identify brain pathologies.
  
• Conduct studies related to prevention and treatment of hyperbilirubinemia and develop strategies to prevent and treat bilirubin-induced brain injury.
  
• Conduct studies to inform optimal nutritional and feeding practices for late-preterm infants and explore their potential role in the etiology of necrotizing enterocolitis.
  
• Conduct studies on the coordination of sucking and swallowing mechanisms, acid secretion, gastroesophageal reflux, and gut motility in late-preterm infants and their overall impact on feeding strategies and hospital discharge practices.
  
• Explore the role of immature gut at late-preterm gestations on later, lifelong gut disorders and milk allergy.
  
• Conduct studies in late-preterm infants to understand how immaturity of the immune system might lead to impaired inflammation and responses to infections.
  
• Conduct studies to understand the effects of preterm birth on developmental immune programming and its role in allergy and asthma in later life.
  
• Conduct studies in developmental pharmacology to explore drug disposition, maturational changes in drug metabolism and elimination, and the factors that induce or inhibit these processes in late-preterm infants.
  

	SUMMARY AND CONCLUSIONS

TOP ABSTRACT DEFINITIONS AND TERMINOLOGIES EPIDEMIOLOGY OBSTETRICAL ISSUES NEONATAL ISSUES SUMMARY AND CONCLUSIONS REFERENCES

The panel underscored the importance of educating health care providers and parents about the vulnerability of late-preterm infants. These infants require diligent evaluation, monitoring, referral, and early return appointments, not only for postneonatal evaluation but also for continued long-term follow-up. The panel suggested a research agenda for the scientific community to consider.

	ACKNOWLEDGMENTS

 
This workshop was sponsored by the National Institute of Child Health and Human Development (NICHD) and the Office of Rare Diseases, National Institutes of Health. The organizers acknowledge support from the Centers for Disease Control and Prevention and the March of Dimes.

The following is a list of conference participants that, along with the conference agenda, is available on the NICHD Web site (www.nichd.nih.gov/about/cdbpm/pp/meetings.htm): Duane Alexander, MD (NICHD, Bethesda, MD), Rachel Avchen, MD (Centers for Disease Control and Prevention [CDC], Atlanta, GA), Susan Bakewell-Sachs, PhD, RN (College of New Jersey School of Nursing, Ewing, NJ), Vinod Bhutani, MD (Stanford University School of Medicine, Stanford, CA), Lillian Blackmon, MD (University of Maryland School of Medicine, Baltimore, MD), Robin Bissinger, MSN, RNC, NNP (National Association of Neonatal Nurse Practitioners [NANN], Goose Creek, SC; Zacharia Cherian, MD (Washington Hospital Center, Washington, DC), Wade D. Clapp, MD (Indiana University Cancer Center, Indianapolis, IN), Reese H. Clark, MD (Pediatrix Medical Group, Inc, Sunrise, FL), Mary D'Alton, MD (Columbia Presbyterian Medical Center, New York, NY), Karla Damus, RN, MSPH, PhD (Albert Einstein College of Medicine and National March of Dimes [MOD], White Plains, NY), Michael Davidoff, MPH (MOD, White Plains, NY), William Allan Engle, MD (Indiana University, Indianapolis, IN), Gabriel Escobar (Kaiser Permanente Medical Center, Walnut Creek, CA), Nancy Green, MD (MOD, White Plains, NY), Gary Hankins, MD (University of Texas Medical Branch, Galveston, TX), James Hanson, MD (NICHD, Bethesda, MD), John Hauth, MD (University of Alabama, Birmingham, Alabama), Rosemary D. Higgins (NICHD, Bethesda, MD), Carl E. Hunt, MD (National Center for Sleep Disorders Research, National Heart, Lung, and Blood Institute, Bethesda, MD), John Ilekis, PhD (NICHD, Bethesda, MD), Lucky Jain, MD (Emory University School of Medicine, Atlanta, GA), Alan H. Jobe, MD, PhD (Cincinnati Children's Hospital Medical Center, Cincinnati, OH), Hannah C. Kinney, MD (Harvard Medical School, Boston, MA), Abbot Laptook, MD (Women and Infant's Hospital, Brown University, Providence, RI), Kenneth Leveno MD (University of Texas Southwestern Medical Center, Dallas, TX), Scott Lorch, MD, MSCE (Children's Hospital of Philadelphia, Philadelphia, PA), Marie McCormick (Harvard University, Boston, MA), Barbara Medoff-Cooper, PhD, FAAN (University of Pennsylvania School of Nursing, Philadelphia, PA), Menachem Miodovnik, MD (Washington Hospital Center, Washington, DC), Joseph Neu, MD (University of Florida, Gainesville, FL), Susan Pagliaro, MA (NICHD, Bethesda, MD), Joann R. Petrini, PhD (MOD, White Plains, NY), Tonse N.K. Raju, MD (NICHD, Bethesda, MD), Uma Reddy, MD (NICHD, Bethesda, MD), Eileen Santa, MA (National Academy of Science, Institute of Medicine, Washington, DC), Anne Santa-Donato, RNC, MSC (Association of Women's Health, Obstetric and Neonatal Nurses, Washington, DC), Richard Schwartz, MD (Maimonides Medical Center, Brooklyn, NY), Carrie K. Shapiro-Mendoza, PhD, MPH (CDC, Atlanta, GA), Baha M. Sibai, MD (University of Cincinnati, Cincinnati, OH), Kathleen Rice Simpson, PhD, RNC, FAAN (St John's Mercy Medical Center, St Louis, MO), Ann R. Stark, MD (Baylor College of Medicine, Houston, TX), Adrienne Stith-Butler, PhD (National Academy of Science, Institute of Medicine, Washington, DC), Catherine Spong, MD (NICHD, Bethesda, MD), Kay Marie Tomashek, MD, MPH (CDC, Atlanta, GA), Carol Wallman, MSN, RNC (NANN, Wellington, CO), Robert M. Ward, MD (University of Utah, Salt Lake City, UT), Marian Willinger, MD (NICHD, Bethesda, MD), and Marshalyn Yeargin-Allsopp, MD (CDC, Atlanta, GA).

	FOOTNOTES

 
Accepted Mar 31, 2006.

Address correspondence to Tonse N.K. Raju, MD, 6100 Executive Blvd, 4B03, Bethesda, MD 20892. E-mail: rajut{at}mail.nih.gov

The opinions expressed in this article are those of the authors and the workshop participants; they do not necessarily reflect the official opinions or positions of the organizations represented by the authors, speakers, or participants.

The authors have indicated they have no financial relationships relevant to this article to disclose.

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