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Table 1 Characteristics of the included studies

From: Global incidence of Necrotizing Enterocolitis: a systematic review and Meta-analysis

Author/year

data base studied

Inclusion criteria

Exclusion criteria

Population at risk reported

NEC case definition

Comment on VLBW

Incidence (cumulative)

Stoll et al. 2010 [18]

NICHD

VLBW infants born in NRN centers GA 22–28 wks.

Congenital anomalies

preterm infants among a VLBW pool

clinically

exclusively VLBW infants

11%

Llanos et al. 2002 [3]

Finger Lakes regional center

all live births in an area of 6 counties. Data obtained from a state-wide registry.

not clear

all newborns in the regional center were accounted for but specific report on NEC stage II and above among the VLBW infants is extracted

NEC stage II and above

population based study but reported specific parameters on VLBW

3.29%

Luig et al. 2005 [4]

New South Wales – state-wide data base. NICUS Neonatal Intensive Care Unit Study

population based study - all preterm infant s between 24 and 28 wks.

not clear

all preterm infants 24–28 weeks of gestation

Clinical definition as confirmed NEC on a set of criteria similar to Bell’s criteria

the mean birth weight and SD of the three epochs were 959 (240), 946 (204), and 935 (240)

7.67%

Holman et al. 2006 [19]

data from discharge registry (the kid’s Inpatient Database) compiled data from 27 states, 2700 hospitals accounting for 10% uncomplicated births from these hospitals

the data is a comprehensive cohort of 10% of all live births in the specified hospitals.

NE after 1 month of age

VLBW infants

ICD 9 -CM code NEC 777.5

Specific report NEC and VLBW infants is presented

exclusively VLBW infants

4.34%

Youn 2015 [16]

Korean Neonatal Network. Admissions into 55 participating neonatal intensive care unites

all live births or admissions within 28 days. VLBW infants. Data collected

52 were diagnosed with NEC II and Spontaneous bowel perforation and were excluded

VLBW infants

bell’s stage II and above

exclusively VLBW infants

6.41%

Qian et al. 2017

95 major referral centers in 29 provinces. Representative of NICU care in the areas

all LBW infants were included.

not specified

the study reports specific parameters of VLBW infants

bell’s stage II and above

reports on VLBW infants are extracted from the publications

2.53%

Ahle et al. 2013 [12]

Swedish National Board of Health and Welfare, the National Patient Register, the Swedish Medical Birth Register and the National Cause of Death Register

all newborns between 1987 and 2009

incomplete identity number

VLBW infants

ICD 9 or ICD 10 code 777F or P77

reported all birth weights. Exact parameters of each weights group are available too

2.68%

Wojkowska-Mach et al. 2014

Polish Neonatal Surveillance Network

all VLBW infants born in PNSS

missing records

VLBW infants

NEC defined according to Gastmeier’s (clinical)

exclusively VLBW

8.68%

Boo et al. 2012 [14]

Malaysian National Neonatal Registry includes NICUs in Malaysia

All VLBW infants in the MNNR.

excluded infants less than 501 g

VLBW infants

bell’s stage II and above

exclusively VLBW infants

6.20%

Wong et al. 2013

Population based study: New South Wales and Australian Capital Territory NICUs included in the NICUS

Low birth weight infants

congenital malformation, syndromes with neurodevelopmental disorders, death in the labor room

low birth weights infants

Bell’s staging criteria

the population was of low birth weights (mean birth weight in two groups was 895 and 917 g.

7.81%

Fanaroff 2003 [20]

NICHD. Retrospective data analysis was performed to compare three epochs.

Registry data

not specified

VLBW infants

not clear

VLBW infants

6.23%

Chedid et al. 2008

Single large Neonatal tertiary referral center

all admission to a single tertiary center in Alain between 2004 and 2006

life threatening malformation, died in labor room, less than 500 g

VLBW infants (exclude less than 500 g

not clear, pneumatosis intestinal or perforation was used a confirmation

all are VLBW

5.78%

Agrawel et al. 2015

data from single largest tertiary hospital in Singapore. Viability threshold less than 25 wks. Gestation

Neonates from High risk VLBW data base with GA < 29 wks.

still birth and miscarriage, less than 23 weeks of gestation

VLBW and pre-term

bell’s stage II and above

exclusively VLBW infants

6.98%

Patole et al. 2016 [21]

single center experience. Comprehensive retrospective cohort comparing a before and after intervention

all neonates less than 34 weeks of gestation within a 2-year period before and after intervention

neonates involved in a clinical trial for the same purpose

the study reported all neonates less than 34 wks. But data on < 28 weeks and epoch 1 were extracted

bell’s stage II and above

the birth weight of the preterm babies was not specifically reported

6.40%

Verstreate et al. 2016

Retrospective cohort study from a single e center using a local audit data base

All neonates in the hospital system

neonates with culture samples that had probably contamination

data on VLBW was extracted only

clinical definition

the data extracted represents exclusively VLBW infants

16.23%

Harkin et al. 2017

Finish Medical Birth Register (preterm < 32 wks.) 22–31. all VLGA 4143

all born less than 32 weeks of gestation

congenital malformations sever chromosomal defects or death before 7 days od life

less than 28 weeks of gestation

clinical criteria

50% less than 1000 g in the entire populations. But weight of the < 28 weeks of gestation was not specified

6.58%

Andersen et al. 2018

birth cohort of the California Office Statewide Health and Development (OSHPD)

all live births with GA 22–36

chromosomal abnormalities

GA less than 28 weeks

ICD-9

no clear specification of the birth weight of the preterm subpopulation

9.10%

Suciu et al. 2017 [22]

From three Romanian hospitals (tertiary centers) data from two different periods 2007–2010 and 2011–2014

all preterm babies less than 28 weeks of gestation

chromosomal abnormalities and birth defects or missing data

preterm babies less than 28 weeks of gestation

bell’s stage II and above

the mean birth and SD of the two epochs were 809 +/−  211 and 958 +/−  149

17.08%

Patel et al. 2016

Prospective 0bservational multicenter birth cohort study evaluating VLBW infants from multiple Level III neonatal centers for exposure blood transfusion (a risk of NEC)

VLBW infants

not specified

VLBW infants

bell’s stage II and above. Cumulative incidence at 8 weeks

exclusively VLBW infants

7.34%

Bajwa et al. 2011 [23]

Swiss Neonatal Network. Double verification by the Swiss Society of Neonatology.

The data set includes all infants < 32 weeks of gestation and > 23 wks.

infants who died in labor room

preterm less than 28 weeks of gestation

clinical definition

no comment on the birth weight of the subpopulation less than 28 weeks of gestation

4.95%

Narang et al. 1993 [24]

Single Neonatal

Intensive Care Unit

All live births during the period January 1986 to September 1990

Not reported

VLBW infants and pretenn infants of gestational

age less than 32 weeks

modified Bell’s criteria

Majority are VLBW infants

1.5%

Lodha 2019 [25]

Tertiary neonatal intensive care units participating in the Canadian Neonatal Network

born at 22 to 28 weeks’ gestational age

birth outside a tertiary-level NICU, moribund at birth, designated as needing palliative care before delivery, had major congenital anomalies, or lacked cord clamping information

22 to 28 weeks’ gestational age

According to the modified Bell criteria, and NEC stage 2 or higher was classified as medical or surgical.

No estimate of the percentage of VLBW infants

9%

Boghossian 2018 [26]

Vermont Oxford Network center

Inborn, singleton infants without congenital malformations

Infants with unknown sex and missing or implausible birth weight

Infants of gestational ages 22 to 29 weeks

diagnosed at surgery or postmortem or required at least 1 clinical sign (eg, bilious gastric aspirate, abdominal distension, or occult blood in stool) and at least 1 radiographic finding (eg, pneumatosis intestinalis, hepatobiliary gas, or pneumoperitoneum).

the mean birth weight and SD of the each weeks reported.

9%

Persson 2018 [27]

7 national networks in high-income countries that are part of the International Neonatal Network for Evaluating Outcomes in Neonates

All singleton infants born alive in high-income countries who were very preterm (24-31 weeks’ gestation) and with a birth weight of less than 1500 g

Multiple pregnancies and major congenital malformations

Very Preterm and Very Low-Birth-Weight Infants

Necrotizing enterocolitis was analyzed in a subgroup of the cohort because data from the UKNC were not available for stage 2 or 3 NEC

Very Preterm and Very Low-Birth-Weight Infants

3%

Suzuki 2018 [28]

Neonatal Research Network

Extremly preterm infants born between 2008 and 2012

Infants who died within 6 days, infants with congenital anomalies, whose sex was undetermined, or whose records were missing data

extremely preterm infants

NEC was defined as stage II/III cases, according to the classifications of Bell

All are VLBW with extremly preterm

4%

Boghossian 2018 [29]

852 US centers participating in the Vermont Oxford Network

Infants born between 154 days (22 weeks and 0 days) and 209 days (29 weeks and 6 days) of gestation

Multiples and infants born with congenital malformations

Large for Gestational Age Infants

NEC was diagnosed at surgery or postmortem or required at least 1 clinical sign (eg, bilious gastric aspirate, abdominal distension, occult blood in stool) and at least 1 radiographic finding (eg, pneumatosis intestinalis, hepatobiliary gas, or pneumoperitoneum)

Mean and SD birth weights reported

7%

Beltempo 2018

Canadian Neonatal Network

Infants born from 22 to 28 weeks’ GA and admitted to 30 Level 3 neonatal intensive care units (NICUs)

Infants moribund on admission or where palliative care was provided at birth due to imminent mortality, infants with major congenital anomalies, and infants with missing SNAP-II

Extremely preterm infants

NEC is defined as stage ≥2 according to Bell’s criteria

Mean and SD birth weights of both cohort is reported

8%