Factors Associated with Low Birth Weight in Indigenous Populations: a systematic review of the world literature

Abstract

Objectives:

we aimed to identify etiological factors for low birth weight (LBW), prematurity and intrauterine growth restriction (IUGR) in the Indigenous Population.

Methods:

for this systematic review, publications were searched in Medline/PubMed, Scopus, Web of Science, and Lilacs until April 2018. The description in this review was based on the PRISMA guideline (Study protocol CRD42016051145, registered in the Centre for Reviews and Dissemination at University of York). We included original studies that reported any risk factor for one of the outcomes in the Indigenous Population. Two of the authors searched independently for papers and the disagreements were solved by a third reviewer

Results:

twenty-four studies were identified, most of them were from the USA, Canada and Australia. The factors associated were similar to the ones observed in the non-indigenous including unfavorable obstetric conditions, maternal malnutrition, smoking, and maternal age at the extremes of childbearing age, besides environmental factors, geographic location, and access to health care in indigenous communities.

Conclusions:

etiologic factors for LBW in Indigenous Population have been receiving little attention, especially in Latin America. The three outcomes showed common causes related to poverty and limited access to healthcare. New studies should ensure explicit criteria for ethnicity, quality on the information about gestational age, and the investigation on contextual and culture-specific variables.

Key words
Indigenous Population; Health Status Disparities; Low birth weight

Resumo

Objetivos:

identificar fatores etiológicos para o baixo peso ao nascer (BPN), prematuridade e crescimento intrauterino restrito (CIUR) em povos indígenas.

Métodos:

revisão sistemática, com pesquisa nas bases Medline/PubMed, Scopus, Web of Science e Lilacs de publicações até abril de 2018. A descrição dessa revisão baseou-se na diretriz PRISMA (Protocolo de estudo CRD42016051145, registrado no Center for Reviews and Dissemination, da Universidade de York). Incluímos estudos originais que relatavam fatores de risco para algum dos três desfechos em Populações Indígenas. Dois autores fizeram buscas independentes e as discordâncias foram solucionadas por um terceiro revisor.

Resultados:

vinte e quatro estudos foram identificados, a maioria deles nos EUA, Canadá e Austrália. Os fatores associados foram semelhantes aos observados nos não indígenas, incluindo condições obstétricas desfavoráveis, desnutrição materna, tabagismo e idade materna nos extremos da idade fértil, além de fatores ambientais, localização geográfica e acesso aos serviços de saúde nas comunidades indígenas.

Conclusões:

os fatores etiológicos para BPN em povos indígenas receberam pouca atenção, especialmente na América Latina. Os três desfechos apresentaram causas comuns relacionadas à pobreza e acesso limitado aos serviços de saúde. Novos estudos devem garantir critérios explícitos para a classificação da etnia, qualidade da informação sobre a idade gestacional e a investigação de variáveis contextuais e culturais dos grupos estudados.

Palavras-chave
População Indígena; Disparidades nos Níveis de Saúde; Baixo peso ao nascer

Introduction

Low birth weight (LBW) is defined as a weight less than 2500g at birth and is an important predictor of unfavorable outcomes in the child’s health such as acute respiratory infections and diarrhea, delay in the growth and development, and child mortality, besides being associated to cardiovascular diseases in adulthood.^1-3 LBW is frequently reported as a prevalent in low life standard populations.⁴

LBW may result from intrauterine growth restriction (IUGR), prematurity, or both.¹ Some studies only analyze factors associated to LBW,^2,5,6 while others investigate specific factors for the incidence of IUGR⁷ or prematurity.^8,9 IUGR has been associated to socioeconomic factors such as low family income, maternal age and marital status, maternal malnutrition (low BMI and height), smoking, and lowquality prenatal care.⁷ Meanwhile, prematurity has been more frequently associated to obstetric conditions like placental abruption and infections, but also to socioeconomic conditions, teenage pregnancy, low maternal schooling and inadequate prenatal care.^8,9 In low and middle income countries, such as Brazil, IUGR and preterm childbirth share several common determinants and its, prevalence tend to be high.⁴

Indigenous Population have precarious living conditions and the worst conditions in health when compared to the general population.^10-12 This population is specially affected by poverty, high prevalence of infectious diseases, particularly at childhood, food insecurity, and limited access to healthcare.^11,18 High prevalence has also been reported for malnutrition, anemia, and smoking in childbearing age women,^11,19 as well as greater proportions of home childbirth and low cesarean rates.²⁰ Although these conditions are related to LBW as a cause or consequence, only few studies have assessed etiological factors for LBW in Indigenous Population worldwide.

For non-indigenous population in Brazil, studies have shown similarities with the international literature in terms of risk factors for LBW. A recent increase in LBW in the country has been related to the growing rates of prematurity due to medical interventions like elective cesareans.^9,21 Despite the broad national and international literature on etiological factors for LBW,^1,2,5,7,16 there are also few specific studies on indigenous population.^13,14 The prevalence of LBW in indigenous children in the country was recently estimated (7.5%) and is similar to the national prevalence of LBW in the general population.¹⁰ However, the prevalence was not estimated by ethnic groups, which can result in inequalities within the indigenous groups.

The combination of multiple risk factors for LBW and the high level of acute respiratory infections, diarrhea, malnutrition, as well as infant mortality in indigenous children reinforce the hypothesis that LBW is a relevant determinant of morbidity and mortality in some indigenous groups in Brazil. However, there may be some differences in the determination of LBW between indigenous and non-indigenous populations, as for example in cesarean rates, and possibly in the contextual factors in these populations. To understand the magnitude of prematurity and IUGR in the composition of LBW in the indigenous population and to identify its etiological factors are essential for intervening effectively in the indigenous health, reducing morbidity and mortality diseases related to poverty.¹¹ The aim of this study was to identify and analyze factors associated to LBW in indigenous children worldwide, characterizing etiological factors associated to prematurity and IUGR.

Methods

Identification and selection of studies

A systematic review was carried out from scientific literature on factors associated to LBW in indigenous population worldwide. Data were collected in April 2018 through a search on Medline/PubMed, Scopus, Web of Science, and Lilacs databases. The description of this review was based on Preferred Reporting Items for Systematic Reviews (PRISMA) guidelines.²² The protocol of the study was registered and published in the Centre for Reviews and Dissemination, University of York (PROSPERO), under the document number CRD42016051145.²³

No limits were considered for the research, such as language or date of publication. The terms for each research database were designed with the assistance of a library scientist.

For the SCOPUS and Medline/PubMed databases, the terms used were: ("Risk Factors" OR "Protective Factors") AND ("Premature Birth" OR "Infant Premature" OR "Fetal Growth Retardation" OR "Infant Low Birth Weight") AND ("Indigenous Infants" OR "Native Children" OR "Indigenous Children" OR "Child* Aborigines" OR "Indigenous Population" OR "Indians Central American" OR "Indians North American" OR "Indians South American" OR "Health of Indigenous Infants" OR "Aborigines, Australian" OR "Native Americans" OR "Inuits" OR "First Nations" OR "Alaska Native" OR "American Indians").

In the Web of Science and Lilacs databases, the terms removed were: "Risk Factors" OR "Protective Factors" and added "Health of Indigenous Infants". In Lilacs, the inclusion of the term Aborigines did not add up to any articles. The inclusion of the terms "population groups", "continental population groups", "tribal", and "etiologic factors" were tested, with no gain in efficiency.

Studies included were based on factors associated to LBW outcomes, prematurity, or IUGR in indigenous populations. Editorials, descriptive articles, and those considering ethnicity as a risk factor, as well as papers which did not present results separately for indigenous individuals were excluded.

Data extraction

The references were managed by Zotero Standalone software. The studies were selected independently by two reviewers and the following stages were included: exclusion of duplicates articles; review of the title and abstract to verify inclusion criteria; full reading of the articles applying the exclusion criteria; and manual search of references from the selected articles by a third reviewer.

A form was used for data extraction with the following information: study identification and author, name of the periodical, and date of publication, data collecting period, sample size, study design, criterion to define ethnicity and its source of information, analyzed outcomes, exposure of the studied variables and the significance of the anaysis model and the control for confounding.

Classification of indigenous population

For the purposes in the study, an attribution of indigenous identity to the child was organized in categories: maternal or paternal ethnicity (selfreported, registered in national or local registries, classified by a health professional, or established by residence in indigenous villages, language spoken, or last name) or the child’s ethnicity as registered in the national health registry.

Methodological quality analysis

The quality of the studies was assessed according to five criteria based on the adapted instrument of Newcastle-Ottawa Scale²⁴ for cohort and case-control studies and the STROBE guidelines for cross-sectional studies:²⁵ (A) used a census or representative probabilistic sample of the target population; (P) having fewer than 20% of losses; (I) having the adjusted LBW by gestational age (GA) or analyzed the IUGR and prematurity separately; (E) having a description of the criteria used to classify the population as indigenous; and (C) having the estimates of the adjusted effect controlling confounded factors. One point was assigned for each fulfilled criterion. The total score could vary from zero to five.

Results

The reference search resulted in the selection of 286 (103 in Scopus, 8 in Web of Science, 110 in Lilacs, and 65 in Medline). After excluding 74 duplicates, 212 titles and abstracts were read and 155 were excluded because they did not fit the eligibility criteria. Afterwards, 57 of them were fully read, 33 were excluded for the reasons shown in Figure 1. The reference manual search of the 23 selected articles resulted in the identification of one more article, totalizing 24 articles in the systematic review (Figure 1).

Figure 1
Flow chart of the systematic review on factors associated to low birth weight in indigenous children.

All the articles for the review were published in English. More than half (14/24 -58.3%) were from the USA and Canada, followed by Australia (6/24 – 25.0%). Only one article from Latin America was identified, it was from Chile. A cross-sectional design was used in 12/24 studies (50.0%), followed by a cohort design (9/24 - 31.8%) (Table 1).

Table 1
Studies identified by author, year of publication, country, and year of data collecting, sample size, and study design.

Author(s)	Year of Publication	Country (year of data collecting)	Total sample indigenous		Study design
			n	%
Abdulrazzaq et al.26	1995	Emirados Árabes Unidos (1992-1993)	3485	100.0	Case-Control
Kieffer et al.27	1995	EUA -Havaí (1979-1990)	7474	100.0	Cross-Sectional
Murphy et al.28	1996	EUA (1989-1991)	8994	100.0	Cross-Sectional
Sayers e Powers29	1997	Austrália (1987-1990)	503	100.0	Cross-Sectional
Rousham e Gracey30	1998	Austrália (1981-1993)	4508	100.0	Cross-Sectional
Abel et al.31	2002	EUA (1978-1992)	156512	8.6	Cross-Sectional
Baldwin et al.32	2002	EUA (1989-1991)	148482	100.0	Cross-Sectional
Emanuel et al.33	2004	EUA (1992-1995)	5626	15.9	Cohort
Muggah et al.34	2004	Canadá (1998-2000)	938	89.0	Cross-Sectional
Heaman et al.35	2005	Canadá (1999-2000)	684	37.7	Case-Control
Gilbreath e Kass36	2006	EUA (1997-2001)	10073	71.0	Cohort
Panaretto et al.37	2006	Austrália (2000-2003)	456	100.0	Cohort
Yang et al.38	2006	China (2003)	1143	100.0	Cross-Sectional
Graham et al.39	2007	Austrália (2001 - 2004)	35240	100.0	Cross-Sectional
Simonet et al.40	2009	Canadá (1989-2000)	2726	100.0	Cohort
Mehaffey et al.41	2010	Canadá (2003-2005)	918	100.0	Cross-Sectional
Wojtyniak et al.42	2010	Groelândia1, Ucrânia e Polônia (2002 - 2004)	1702	35.1	Cohort
Coughlin et al.43	2013	EUA (1998-2008)	4149	100.0	Cohort
England et al.44	2013	EUA-Alaska (1997-2005)	1104	100.0	Case-Control
Dorfman et al.45	2015	EUA-Alaska (2004-2011)	12420	100.0	Cohort
Rothhammer et al.46	2015	Chile (2004-2010)	5295	24.2	Cross-Sectional
Brown et al.47	2016	Austrália (2011-2013)	337	100.0	Cross-Sectional
Oster e Toth48	2016	Canadá (2000-2009)	426945	6.6	Cohort
Kildea et al.49	2017	Austrália (2004-2006/2009-2011)	713	100.0	Cohort

• ¹
  Only the data from Greenland were used, the only country that studied indigenous population (Inuit).

In most of the studies, the authors defined the newborns as indigenous based on secondary registrations of the infants or of their parents (local or national information systems, the father’s and/or the mother’s birth certificate, and the mother’s medical record. Fourteen of the 24 studies failed to specify the classification criteria for ethnicity. Of the 24 studies, only 3 attributed to the child’s ethnicity by the mother’s or father’s selfdeclared at the time of the study, in other words, as a primary data source (Table 2).

Table 2
Source of information , form and attribution and classification for the child's race/ethnicity.

References	Source of information on race and / or ethnicity	Criterion for the child's race and / or ethnicity	Race / Ethnicity
Abdulrazzaq et al.26	Maternal medical file	Not specified	Indigenous Population/ Bedouins
Kieffer et al.27	National live births database	Maternal ethnicity registered on mother's birth certificate	Samoan and Hawaiian
Murphy et al.28	National live births database	Not specified	Alaska Native
Sayers e Powers29	Interview with mother	Self-reported maternal ethnicity	Aboriginal
Rousham e Gracey30	Regional health monitoring program	Not specified	Aboriginal
Abel et al.31	Maternal classification in information systems of the State Health Department	Not specified	Native American
Baldwin et al.32	Mother's or father's birth registration in the national information system	Not specified	American /Alaska Natives
Emanuel et al.33	Birth certificate	Not specified	Native Americans
Muggah et al.34	Hospital registrations	Maternal ethnicity classified by health professional	Inuit
Heaman et al.35	Interview with mother in hospital after childbirth	Self-reported maternal ethnicity	Aboriginal
Gilbreath e Kass36	Vital statistics bank	Maternal ethnicity defined by residence in federally acknowledged native villages	Alaska Native
Panaretto et al.37	National live births bank	Self-reported maternal or paternal ethnicity	Aboriginal and Torres Strait Natives
Yang et al.38	Hospital registrations	Not specified	Aboriginal
Graham et al.39	Maternal ethnicity in national bank of perinatal data	Not specified	Aboriginal and Torres Strait Natives
Simonet et al.40	Identification of mother tongue in national vital statistics bank	Maternal ethnicity defined by language spoken by mother	Inuit
Mehaffey et al.41	Hospital registrations	Not specified	Inuit
Wojtyniak et al.42	Interview with mother and partner	Not specified	Inuit
Coughlin et al.43	Mother or father's registration in a federally recognized tribe in the national birth registry	Paternal or maternal ethnicity registered in federally acknowledged village	American Indian
England et al.44	Hospital registrations	Not specified	Alaska Native
Dorfman et al.45	Birth certificate	Not specified	American Indians/Alaska Natives
Rothhammer et al.46	Hospital registrations	Maternal ethnicity defined according to mother's last name	Aymara
Brown et al.47	Interview or filling out questionnaire	Not specified	Aboriginal and/or Torres Strait Natives
Oster e Toth48	Health insurance plan registrations	Ethnicity registered on health insurance plan	First Nations and Inuit
Kildea et al.49	Health centers registrations	Not specified	Aboriginal

Only four articles met all the established quality criteria, and nine did not meet any of the quality criteria. Nine articles studied birth weight without adjusting for GA or differentiating between prematurity and IUGR. In six studies, no adjustment was made for the confounding variables, and three of them only made comparisons between proportions or means. Among the five criteria adopted to analyze the quality of the articles, the worst one was the description of the criteria used to classify ethnicity (Table 3).

Table 3
Studies identified in bibliographic research according to outcome, the use of statistical analysis, and quality assessment.

References	Outcome	Statistical analysis	Quality assessment1
			A	P	I	E	C	Total
Oster e Toth48	LBW	Logistic regression and multiple linear	1	1	1	1	1	5
Coughlin et al.43	LBW; Prematurity; SGA	Multiple logistic regression	1	1	1	1	1	5
Simonet et al.40	LBW; Prematurity; SGA	Multilevel logistic regression	1	1	1	1	1	5
Panaretto et al.37	LBW; Prematurity; SGA	Multiple logistic regression	1	1	1	1	1	5
Heaman et al.35	Prematurity	Multiple logistic regression.	1	0	1	1	1	4
Kieffer et al.27	Birth weight	Logistic regression and multiple linear	1	1	0	1	1	4
Wojtyniak et al.42	Birth weight; Prematurity	Logistic regression and multiple linear	1	1	1	0	1	4
Graham et al.39	LBW; prematurity	Multiple logistic regression	1	1	1	0	1	4
England et al.44	Prematurity	Multiple logistic regression	1	1	1	0	1	4
Brown et al.47	LBW; Prematurity; SGA	Multiple logistic regression	1	1	1	0	1	4
Kildea et al.49	LBW; prematurity; SGA	Multiple logistic regression	1	1	1	0	1	4
Muggah et al.34	Prematurity	Pearson correlation and ANOVA (bivariate)	1	1	1	1	0	4
Dorfman et al.45	Prematurity	Multiple logistic regression	1	1	1	0	1	4
Gilbreath e Kass36	Birth weight	Covariance multivariate analysis	1	0	0	1	1	3
Rothhammer et al.46	Birth weight	Comparison of means2	1	1	0	1	0	3
Baldwin et al.32	LBW	Multiple logistic regression	1	1	0	0	1	3
Mehaffey et al.41	LBW; Prematurity; SGA	Univariate logistic regression	1	1	1	0	0	3
Simonet et al.40	LBW; prematurity; IUGR	Multiple logistic regression	0	0	1	1	1	3
Abel et al.31	LBW; Prematurity	Multiple logistic regression	1	0	1	0	1	3
Abdulrazzaq et al.26	LBW	Univariate logistic regression	1	1	0	0	0	2
Emanuel et al.33	LBW	Multiple correlation	1	0	0	0	1	2
Yang et al.38	LBW	Multiple logistic regression	0	1	0	0	1	2
Rousham e Gracey30	Birth weight	Univariate logistic regression	1	1	0	0	0	2
Murphy et al.28	Birth weight	Comparison of means (t-test)	1	0	0	0	0	1
Total articles per item			22	18	15	10	18	-

• ¹
  (A) census or representative probabilistic sample of the target population; (P) proportion of losses less than 20%; (I) adjustment performed for gestational age or differentiated between prematurity and SGA/IUGR as outcomes; (E) description of the criterion used to classify the population as indigenous; (C) adjusted effects estimates with control for confounding factors.
• ²
  Study describes that it performed multiple regression, but did not show the results, the table only shows the comparison among means.

Table 4 and 5 show the variables explored as factors associated to LBW, prematurity, and IUGR and the respective measures of association. The most frequently studied variables were: maternal smoking, evaluate mainly the number of cigarettes smoked per day, followed by maternal age.

Table 4
Obstetric and maternal factors associated to LBW, prematurity and IUGR, with association measurements, CI95% or p.

Associated factors	References	Birth weight		Prematurity		IUGR / SGA
		Association Measurement	CI / p	Association Measurement	CI / p	Association Measurement	CI / p
Obstetric factors
Prolonged rupture of membranes	Sayers e Powers29	-	-	OR= 18.7*	5.9 - 59.7	-	-
Premature rupture of membranes	Abdulrazzaq et al.26	OR= 6.2	1.3 - 27.04	-	-	-	-
	Gilbreath e Kass36	-	-	OR= 12.7*	5.31 - 30.39	-	-
Primiparous (and ≥18 years)	Kieffer et al.27	β= - 151.3*	p<0.01	-	-	-	-
		OR= 1.43*	1.05 - 1.94	-	-
Parity 0 (Ref.1 or 2 children)	Oster e Toth48	OR= 1.07*	1.02 - 1.13	-	-	-	-
Parity (Ref. Multiparous)	Kildea et al.49	OR= 3.06*	1,68 - 5.58	NS	NS	OR=1.89*	1.25 - 2.86
Parity (and ≥18 years)	Kieffer et al.27	β= 142.0*	p<0.01	-	-	-	-
Multiple gestation	Oster e Toth48	OR= 16.31*	14.0 - 19.0	-	-	-	-
Pregnancy-induced hypertension	Sayers e Powers29	NS	NS	OR= 12.7*	5.2 - 30.9	NS	NS
	Heaman et al.35	-	-	OR= 7.51*	2.11 - 26.76	-	-
	Panaretto et al.37	NS	NS	NS	NS	POR= 6.1*	1.8 - 20.4
	Dorfman et al.45	-	-	OR= 1.89	1.49 - 2.40	-	-
	Panaretto et al.37	POR= 8.2*	1.7 - 40.3	NS	NS	POR= 7.4*	1.1 - 50.1
Pre-history of stillbirth	Panaretto et al.37	POR= 7.6*	2.5 - 22.8	NS	NS	NS	NS
	Oster e Toth48	OR= 2.18*	1.73 - 2.74	-	-	-	-
History of LBW	Abdulrazzaq et al.26	OR= 2.23	1.48 - 3.33	-	-	-	-
	Oster e Toth48	OR= 1.40*	1.20 - 1.63	-	-	-	-
Pre-history of neonatal death	Oster e Toth48	OR= 1.55*	1.11 - 2.17	-	-	-	-
Pre-history of prematurity	Oster e Toth48	OR= 1.76*	1.59 - 1.94	-	-	-	-
	Heaman et al.35	-	-	OR= 4.32*	1.67 - 11.22	-	-
	Panaretto et al.37	NS	NS	POR= 18.5*	6.7 - 51.2	-	-
	Kildea et al.49	NS	NS	OR= 2.07*	1.26 - 3.41	NS	NS
Pre-history of Small to GA	Oster e Toth48	OR= 3.64*	2.60 - 5.09	-	-	-	-
Diabetes	Dorfman et al.45	-	-	OR= 1.83*	1.21 - 2.78	-	-
Diabetes or HBP	Graham et al.39	OR= 1.44*	1.32 - 1.57	NS	NS	-	-
Preexisting HBP	Oster e Toth48	OR= 3.44*	2.39 - 4.94	-	-	-	-
Chronic renal disease	Oster e Toth48	OR= 3.18*	1.23 - 8.18	-	-	-	-
Antepartum hemorrhage and placental complication	Kildea et al.49	-	-	OR= 5.59*	2.49 - 12.56	-	-
Hospitalization during pregnancy	Heaman et al.35	-	-	OR= 3.27*	1.28 - 8.33	-	-
Other obstetric problems	Sayers e Powers29	NS	NS	OR= 15.7*	5.0 - 44.9	NS	NS
Maternal behavioral factors:
Maternal smoking	Oster e Toth48	OR= 1.29*	1.17 - 1.43	-	-	-	-
	Graham et al.39	OR= 1.80*	1.66 - 1.95	NS	NS	-	-
	Mehaffey et al.41	OR= 3.8	1.4 - 10.5	NS	NS	OR= 2.5	1.1 - 5.4
	Panaretto et al.37	NS	NS	NS	NS	OR= 3.7*	1.2 - 11.4
No (reference)	Kildea et al.49	NS	NS	1	1	NS	NS
Yes	Kildea et al.49	NS	NS	OR= 1.00	0.58 - 1.74	NS	NS
Not Registered	Kildea et al.49	NS	NS	OR= 3.35*	1.90 - 5.89	NS	NS
>10 cigarettes a day	-	OR= 6.7	2.3 - 19.6	OR= 2.1	1.1 - 4.2	OR= 3.7	1.6 - 8.8
>1/2 pack a day	Sayers e Powers29	OR= 2.8*	1.3 - 6.1	NS	NS	OR= 1.8*	1.1 -3.0
Betel chewing	Yang et al.38	OR= 1.7*	1.07 - 2.72	-	-	-	-
Alcohol use	Oster e Toth48	OR= 1.45*	1.26 - 1.67	-	-	-	-
Maternal behavioral factors
Alcohol abuse	Panaretto et al.37	NS	NS	NS	NS	POR= 7.4*	1.1 - 50.1
Drug use	Oster e Toth48	OR= 2.05*	1.76 - 2.39	-	-	-	-
Marijuana use during pregnancy	Brown et al.47	OR= 3.9*	1.4 - 11.2	NS	NS	NS	NS
Maternal nutrition
Maternal BMI <18.5 (postpartum)	Sayers e Powers29	OR= 5.1*	2.1 - 12.0	NS	NS	OR= 2.5*	1.4 - 4.6
Maternal BMI>25 (1st prenatal visit)	Panaretto et al.37	1.0	-	1.0	-	NS	NS
Maternal BMI 20 to 24.9		NS	NS	POR= 2.0*	1.2 - 3.2	NS	NS
Maternal BMI<20		POR= 5.5*	2.0 - 14.6	POR= 4.9*	1.5 - 15.9	NS	NS
Maternal birth weight	Emanuel et al.33	R2= 3.87%	p<0.001	-	-	-	-
Maternal height	Emanuel et al.33	R2= 4.16%*	p<0.001	-	-	-	-
Low gestational weight gain (<9.1kg)	Heaman et al.35	-	-	OR= 8.95*	1.86 - 42.94	-	-
Pre-gestational weight	Emanuel et al.33	R2= 6.16%*	p<0.001	-	-	-	-
Pre-gestational weight<45kg	Oster e Toth48	OR= 1.82*	1.01 - 2.99	-	-	-	-
Pre-gestational weight>91kg	Oster e Toth48	OR= 0.54*	0.46 - 0.64	-	-	-	-
Anemia (ref. No)	Kildea et al.49	NS	NS	OR= 0.51*	0.33 - 0.80	NS	NS
Prenatal
Inadequate prenatal care	Wells et al.24	β= 43.3*	p<0.01	-	-	-	-
≤ 3 prenatal consultations	Panaretto et al.37	NS	NS	POR= 3.4*	1.4 - 8.1	NS	NS
Recommended number of antenatal consultations (Ref.yes)	Kildea et al.49	NS	NS	OR= 2.16*	1.27 - 3.42	NS	NS
Childbirth conditions:
History of cesarean	Oster e Toth48	OR= 1.24*	1.09 - 1.42	-	-	-	-

• ^*
  Variables that were adjusted in multiple models.
• ¹R²: multiple correlation coefficients; OR= Odds Ratio; NS= Non significant; POR= Prevalence Odds Ratio.

Table 5
Sociodemographic and environmental factors associated to LBW, prematurity, and IUGR, with association measurements, CI95% or p.

Associated factors	References	Birth weight		Prematurity		IUGR / SGA
		Association Measurement	CI / p	Association Measurement	CI / p	Association Measurement	CI / p
Infant 's Sex (ref. Male)	Kieffer et al.27	OR=2.10*	1.17 - 3.78	OR= 1.74*	1.12 - 2.69	NS	NS
Maternal characteristics:
Mother single	Oliveira et al.51	β= -67.5*	p<0.01	-	-	-	-
age <20 years	Santos et al.53	NS	NS	NS	NS	OR= 1.9*	1.2 - 2.9
age <19 years	Gilbreath e Kass36	-	-	OR= 0.19*	0.04 - 0.89	-	-
age ≥18 years and primiparous	Oliveira et al.51	β= -151.3*	p<0.01	-	-	-	-
		OR= 1.43*	1.05 - 1.94	-	-	-	-
age ≥18 years and high parity	Oliveira et al.51	β= 142.0*	p<0.01	-	-	-	-
age 17 years	Abdulrazzaq et al.26	OR= 0,76*	0.62 - 0.94	-	-	-	-
age ≥35 years	Abdulrazzaq et al.26	OR= 1.61*	1.39 - 1.87	-	-	-	-
age 18 to 34 years	Abdulrazzaq et al.26	1.00	-	-	-	-	-
age 21 to 24 years	Oster e Toth48	-	-	1.00	-	-	-
age ≥35 years	Oster e Toth48	-	-	OR= 2.09	1.45 - 3.00	-	-
age <20 years	Kieffer et al.27	NS	NS	OR= 1.69*	1.04 - 2.76	NS	NS
age 20-34	Kieffer et al.27	NS	NS	1.00	-	NS	NS
High schooling	Abel et al.31	β= 75.2*	p<0.01	-	-	-	-
		OR= 0.61*	0.41 - 0.92	-	-	-	-
Education >12 years	-	-	-	1.00	-	-	-
Education 12 years	Oster e Toth48	-	-	OR= 1.38	1.08 - 1.76	-	-
Education <12 years	-	-	-	OR= 1.58	1.22 - 2.05	-	-
Physical abuse with lesions	Abel et al.31	OR= 2.43*	1.06 - 5.55	-	-	-	-
Environmental conditions
Maternal serum CB 153 concentration	Sayers e Powers29	β= -59.2*	-100.6 / -17.8	NS	NS	-	-
Maternal serum p.p-DDE log concentration	Sayers e Powers29	β= -56.0*	-99.5 / -12.5	NS	NS	-	-
Open dumpsite in village -Low contamination	Wojtyniak et al.42	Reference	-	-	-	-	-
High contamination	Wojtyniak et al.42	Mean Dif.= -77.3*	-138.1 / 16.6	-	-	-	-
Rainy season (Birth weight<1500g)	Murphy et al.28	OR= 2.73	2.03 - 3.67	-	-	-	-
Dry season	Murphy et al.28	1	-	-	-	-	-
Living in rural area	Kildea et al.49	OR= 0.89*	0.85 -0.93	-	-	-	-
Living in remote area	Baldwin et al.32	OR= 1.09*	1.01 - 1.19	NS	NS	-	-
Socioeconomic factors
Grouped socioeconomic factors (maternal age, parity, schooling, and prenatal care)	Dorfman et al.45	R2= 9.53%*	p<0.001	-	-	-	-
Paternal age	England et al.44	OR= 1.04*	1.01 - 1.08	NS	NS	-	-
Participant in HS2, does not live in difficult-to-reach access area	Brown et al.47	OR= 0.37*	0.14 - 0.96	NS	NS	NS	NS

• ^*
  Variables that were adjusted in multiple models.
• ¹R²= multiple correlation coefficients.
• ²Healthy Start Program (HS) - Each HS works within a specific tribal service area. All the clients will receive a nurse's visit to assess the individualized, medical, social, and educational needs based on the risks identified, referrals for the necessary services, monthly home visits during pregnancy, and additional services according to as needed. OR= Odds Ratio; NS= Non significant; POR= Prevalence Odds Ratio.

Considering only the variables adjusted for confounding, the main risk factors for prematurity were: obstetric conditions such as prolonged and premature rupture of the membranes, pregnancyinduced hypertension, diabetes and obstetric history of prematurity; hospitalization during pregnancy; maternal malnutrition, defined as pre-gestational maternal BMI <20, low gestational weight gain (<9.1kg) or anemia; low number of prenatal consultations; and low maternal age (<19 years) as a protective factor. For IUGR featured smoking and alcohol abuse during pregnancy; maternal malnutrition (BMI <18.5); obstetric conditions like pregnancy-induced hypertension and urinary tract infection; and low maternal age (<20 years).

Factors associated to LBW included the same ones as for prematurity and IUGR, plus featuring those related to specific indigenous environmental contexts, like inadequate waste disposal; environmental contamination with persistent organic pollutants; rainy season (versus dry seasons); reside in villages located in rural or remote areas; and have limited access to health services.

Discussion

The studies identified in this review were concentrated in 3 countries (Australia, Canada, and USA).

This fact does not only restrict itself to studies on birth weight, but also studies were observed on adverse pregnancy or neonatal outcomes in indige-nous populations.^15,48 These studies are rare in Latin America although 10% of its population may be indigenous and the region concentrates one of the greatest ethnic diversities in the world.¹²

The literature on etiological factors for LBW in indigenous population is incipient, especially when comparing to non-indigenous population. However, there are similarities between the two groups about factors associated to LBW, prematurity and IUGR.

IUGR has been reported as the main component of LBW in indigenous population,⁴⁸ unlike the observations made in the general population. Nevertheless, this outcome was only studied in 7 of the 24 studies. IUGR was associated to maternal smoking and alcohol abuse, maternal malnutrition, and hypertension and infections in the pregnancy, all these factors are considered to be modifiable by improving the living conditions and having access to health services. On the other hand, prematurity was investigated in more than half of the studies in this review, and its etiological factors were mostly obstetric conditions. The low cesarean rates in indigenous population^20,49 indicate that prematurity in these groups may result in a spontaneous premature delivery, resulting in an adverse obstetric conditions, maternal malnutrition, and limited access to prenatal care.⁸ Spontaneous premature childbirth has complex and multifactorial causes related to infections or inflammations in pregnancy, besides economic and social vulnerability, which are highly prevalent conditions in indigenous peoples.^8,9,11

Maternal smoking was a risk factor most frequently associated to LBW in indigenous population. Sayers and Power²⁹ reported 18% attributable the risk of industrialized cigarettes for the LBW outcome and 10% for IUGR. Mehaffey et al.⁴¹ investigated smoking in the first trimester of pregnancy and identified a significant doseresponse effect for the three investigated outcomes (LBW, prematurity, and IUGR), even though the associations were only estimated as gross. However, other studies that presented adjusted estimates have reiterated this association.^{29,34,38-40,47}

The difficulty in measuring tobacco exposure is a problem in the studies with indigenous populations.^26,35 Difficulties are reported in quantifying the number of cigarettes smoked, since industrialized tobacco tends to be used intermittently and depends on the availability of monetary resources. It is also difficult to measure the consumption of tobacco in other forms, such as chewing, domestic preparations with or without mixing other substances,³⁵ and pipe smoking for recreational or religious purposes.⁵⁰ Thus, studies on factors associated to LBW in indigenous population should develop strategies to measure accurately, in different contexts, the type of tobacco consumed, doses, periods, and the duration of exposure during pregnancy.

Some studies found in this review describe an inverse association between maternal age and LBW, which is commonly reported in non-indigenous populations.^2,6,51 In the Western societies, this association has been attributed to biological immaturity in adolescence and social determinants such as inadequate prenatal care and fragile social support networks, or pregnancy rejection by the family or the partner.⁵¹ However, two studies found a direct association between LBW and maternal age.^30,35 The authors discussed that the indigenous women’s health deteriorates more rapidly with age due to the conditions of poverty and high fertility. A second hypothesis emerged from a community focus group, when it was reported that younger pregnant women tend to receive more family and community support.

The effect of maternal age on LBW can differ according to the level of development in the country and its regions. In population with high socioeconomic status and adequate prenatal care, the negative perinatal effects of maternal age are minimized, reinforcing the relation between LBW and social and economic factors, especially in women under 20 years old.^52,53 Such findings suggest that the effect of maternal age can be expressed in different ways, depending on the local contexts. For example, in different indigenous communities, pregnancy before 20 years of age is not viewed negatively,⁵⁴ which could explain the direct association between maternal age and LBW found in the two studies.

Low maternal BMI and low pre-gestational maternal weight were associated to LBW. A study carried out on aborigines in Australia²⁹ found an inverse association between postpartum maternal BMI and LBW. The authors discussed that the prevalence of maternal malnutrition would be higher if measured in early pregnancy, recommending nutritional rehabilitation of pregnant women to reduce the risk of fetal malnutrition.²⁹ In the same line, a study on indigenous population in Manitoba, Canada,³⁵ showed an association between low gestational weight gain and prematurity.

In relation to environmental factors, a study carried out in Alaska showed that a mean birth weight was lower in indigenous villages that lacked adequate trash disposal. This effect probably resulted on water and soil contamination and inhalation of potentially toxic smoke due to burning residues.³⁶

Another environmental factor studied was the seasonality. Children born in the rainy season were more likely to have been born with very low birth weight (<1,500g), due to the scarcity and difficult access to food, crowding, and confinement in the home and higher risk of environmental contamination and infection. This scenario reinforces the hypothesis that LBW results from the adverse socioeconomic and environmental situations to which indigenous population are exposed.³⁰

Living in rural areas showed controversial effects in relation to the risk of LBW. According to Baldwin et al.³², close and permanent contact with urban centers can result in worse living conditions for indigenous population. Villages located close to urban centers tend to have smaller territories, limiting their food plantation, hunting and fishing. However, Graham et al.³⁹ reported higher risk of LBW in remote areas due to greater difficulty in access to the health services, as prenatal care. Coughlin et al.⁴³ observed an attenuation of this effect when the community has access to health services, particularly when it is located in the village and culturally adapted.

The investigation of environmental factors has advanced and proven to be relevant in the studies on the determination of LBW in indigenous populations.^{32,37,39,43,45} In the other hand, socioeconomic factors^34,38,49 have received little attention, demonstrating to be less relevant in the determination of LBW. A possible explanation is the relative socioeconomic homogeneity of indigenous groups,³⁰ which is not possible to capture this differentiation with the usual socioeconomic indicators. This would require the development of more sensitive indicators to capture the inequalities in different indigenous contexts.

Six of the 24 articles were methodologically less robust, since they did not adjust for confounding, although their results are consistent with the literature in non-indigenous populations. We would like to highlight the frequent lack of information on the methods or criteria in defining indigenous individuals. According to Smyliea and Firestone,⁵⁵ this fact limits the interpretation of the results, since the allocation of indigenous individuals to other racial or ethnic categories and vice versa underestimates the inequalities in the health indicators between indigenous and non-indigenous groups, limiting the identification of needs and contributing to the marginalization of these people.¹⁰ In addition, explicit criteria allow better comparability among studies and facilitates the understanding of the studied contexts.

Therefore, considering to be essential, studies on etiological factors for LBW in indigenous population present adjusted association measurements which specify the methods for racial ethnic classification, and inform gestational age (GA), indicating the sources and its form to estimate. Studies are needed to ensure the best source of data collection on GA, since correct GA is essential to differentiate between LBW due to prematurity and LBW due to IUGR, and such information is still scarce for indigenous populations worldwide.^30,37 New studies should be recommended for further examine specific contextual variables in these populations, as climate and environmental conditions, location and type of housing, proximity to urban centers, structure and organization of local health services, and culture-specific behavioral factors as tobacco and other substances use and exposure to pollutants and contaminants.

Conclusions

Low birth weight has received little attention in indigenous population when compared to the non-indigenous population, and Latin America is considered the poorest and most populous regions and, is underrepresented. The risk factors identified in the review are similar to those of the general population as obstetric causes, maternal nutritional conditions, access to health services, and environmental conditions, and are modifiable by actions of the health services in partnership with other sectors.

Prematurity and IUGR show common causes related to poverty and limited access to health services. The studies lack quality and methodological clarity on relevant aspects in order to guarantee their comparability. More studies are necessary on factors related to LBW in indigenous population in Latin America. Investment is needed to have access in the highquality prenatal care and to decrease the prevalence of prematurity and IUGR related to morbidity and mortality among the indigenous population.

References

• ¹
  Barros FC, Victora CG, Matijasevich A, Santos IS, Horta BL, Silveira MF, Barros AJD. Preterm births, low birth weight, and intrauterine growth restriction in three birth cohorts in Southern Brazil: 1982, 1993 and 2004. Cad Saúde Pública. 2008; 24: S390-S8.
• ²
  Ganesh Kumar S, Harsha Kumar HN, Jayaram S, Kotian MS. Determinants of low birth weight: A case control study in a district hospital in Karnataka. Indian J Pediatr. 2010; 77 (1): 87-9.
• ³
  Arnold L, Hoy W, Wang Z. Low birthweight increases risk for cardiovascular disease hospitalisations in a remote Indigenous Australian community - a prospective cohort study. Aust N Z J Public Health. 2016; 40 (Suppl 1): S102-S6.
• ⁴
  Barros FC, Barros AJD, Villar J, Matijasevich A, Domingues MR, Victora CG. How many low birthweight babies in low- and middle-income countries are preterm? Rev Saúde Pública. 2011; 45 (3): 607-16.
• ⁵
  Monteiro CA, Benicio MHD, Ortiz LP. Tendência secular do peso ao nascer na cidade de São Paulo (1976-1998). Rev Saúde Pública. 2000; 34 (Supl 6): 26-40.
• ⁶
  Barbas D da S, Costa AJL, Luiz RR, Kale PL. Determinantes do peso insuficiente e do baixo peso ao nascer na cidade do Rio de Janeiro, Brasil, 2001. Epidemiol Serv Saúde. 2009; 18 (2): 161-70.
• ⁷
  Zambonato AMK, Pinheiro RT, Horta BL, Tomasi E. Fatores de risco para nascimento de crianças pequenas para idade gestacional. Rev Saúde Pública. 2004; 38 (1): 24-9.
• ⁸
  Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. The Lancet. 2008; 371 (9606): 75-84.
• ⁹
  Leal MC, Esteves-Pereira AP, Nakamura-Pereira M, Torres JA, Theme-Filha M, Domingues RMSM, Dias MAB, Moreira ME, Gama SG. Prevalence and risk factors related to preterm birth in Brazil. Reprod Health. 2016; 13 (Suppl 3): 163-74.
• ¹⁰
  Anderson I, Robson B, Connolly M, Al-Yaman F, Bjertness E, King A, Tynan M, Madden R, Bang A, Coimbra Jr. CEA, et al Indigenous and tribal peoples' health (The Lancet-Lowitja Institute Global Collaboration): a population study. The Lancet. 2016; 388 (10040): 131-57.
• ¹¹
  Gracey M, King M. Indigenous health part 1: determinants and disease patterns. The Lancet. 2009; 374 (9683): 65-75.
• ¹²
  Montenegro RA, Stephens C. Indigenous health in Latin America and the Caribbean. The Lancet. 2006; 367 (9525): 1859-69.
• ¹³
  Cardoso AM, Coimbra CE, Werneck GL. Risk factors for hospital admission due to acute lower respiratory tract infection in Guarani indigenous children in southern Brazil: a population-based case-control study. Trop Med Int Health. 2013; 18 (5): 596-607.
• ¹⁴
  Cardoso AM, Horta BL, Santos RV, Escobar AL, Welch JR, Coimbra CEA. Prevalence of pneumonia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Int Health. 2015; 7 (6): 412-9.
• ¹⁵
  Sayers SM. Indigenous Newborn Care. Pediatr Clin North Am. 2009; 56 (6): 1243-61.
• ¹⁶
  Kramer MS. Determinants of low birth weight: metho-dological assessment and meta-analysis. Bull World Health Organ. 1987; 65 (5): 663-737.
• ¹⁷
  Cardoso AM, Coimbra Jr. CEA, Barreto CTG, Werneck GL, Santos RV. Mortality among Guarani Indians in Southeastern and Southern Brazil. Cad Saúde Pública. 2011; 27 (Suppl 2): S222-S36.
• ¹⁸
  Cardoso AM, Coimbra Jr. CEA, Tavares FG. Morbidade hospitalar indígena Guarani no Sul e Sudeste do Brasil. Rev Bras. Epidemiol. 2010; 13 (1): 21-34.
• ¹⁹
  Lício JSA, Fávaro TR, Chaves CRM de M. Anemia em crianças e mulheres indígenas no Brasil: revisão sistemática. Ciênc Saúde Colet. 2016; 21 (8): 2571-81.
• ²⁰
  ABRASCO. Inquérito Nacional de Saúde e Nutrição dos Povos Indígenas. Relatório Final (Análise dos Dados). [acesso em 20 Janeiro de 2018]. Disponível em: http://ecos-redenutri.bvs.br/tiki-download_file.php?fileId=1284
  » http://ecos-redenutri.bvs.br/tiki-download_file.php?fileId=1284
• ²¹
  Leal M do C, Esteves-Pereira AP, Nakamura-Pereira M, Torres JA, Domingues RMSM, Dias MAB, Moreira ME, Theme-Filha M, Gama SGN. Provider-Initiated Late Preterm Births in Brazil: Differences between Public and Private Health Services. PLoS ONE. 2016; 19 11(5): e0155511.
• ²²
  Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009; 6 (7): e1000097.
• ²³
  National Institute for Health Research. International prospective register of systematic reviews. [acesso em 15 dez 2016]. Disponível em: https://www.crd.york.ac.uk/ PROSPERO/index.php
  » https://www.crd.york.ac.uk/ PROSPERO/index.php
• ²⁴
  Wells G, Shea B, O'Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non randomised studies in meta-analyses. [acesso em 2 fev 2017]. Disponível em: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  » http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
• ²⁵
  Malta M, Cardoso LO, Bastos FI, Magnanini MMF, Silva CMFP. Iniciativa STROBE: subsídios para a comunicação de estudos observacionais. Rev Saúde Pública. 2010; 44 (3): 559-65.
• ²⁶
  Abdulrazzaq Y, Bener A, Dawodu A, Kappel I, Surouri FA, Varady E, Liddle L, Varghese M, Cheema MY. Obstetric risk factors affecting incidence of low birth weight in live-born infants. Biol Neonate. 1995; 67 (3): 160-6.
• ²⁷
  Kieffer EC, Alexander GR, Mor JM. Pregnancy outcomes of Pacific Islanders in Hawaii. Am J Epidemiol. 1995; 141 (7): 674-9.
• ²⁸
  Murphy NJ, Butler SW, Petersen KM, Heart V, Murphy CM. Tobacco erases 30 years of progress: preliminary analysis of the effect of tobacco smoking on Alaska Native birth weight. Alaska Med. 1996; 38 (1): 31-3.
• ²⁹
  Sayers S, Powers J. Risk factors for aboriginal low birth weight, intrauterine growth retardation and preterm birth in the Darwin Health Region. Aust N Z J Public Health. 1997; 21 (5): 524-30.
• ³⁰
  Rousham EK, Gracey M. Seasonality of low birthweight in indigenous Australians: an increase in pre-term birth or intrauterine growth retardation? Aust N Z J Public Health. 1998; 22 (6): 669-72.
• ³¹
  Abel EL, Kruger M, Burd L. Effects of maternal and paternal age on Caucasian and Native American preterm births and birth weights. Am J Perinatol. 2002; 19 (1): 49-54.
• ³²
  Baldwin L-M, Grossman DC, Casey S, Hollow W, Sugarman JR, Freeman WL, Hart LG. Perinatal and infant health among rural and urban American Indians/Alaska Natives. Am J Public Health. 2002; 92 (9): 1491-7.
• ³³
  Emanuel I, Kimpo C, Moceri V. The association of maternal growth and socio-economic measures with infant birth-weight in four ethnic groups. Int J Epidemiol. 2004; 33 (6): 1236-42.
• ³⁴
  Muggah E, Way D, Muirhead M, Baskerville B. Preterm delivery among Inuit women in the Baffin Region of the Canadian Arctic. Int J Circumpolar Health. 2004; 63 (Suppl 2): 242-7.
• ³⁵
  Heaman MI, Blanchard JF, Gupton AL, Moffatt MEK, Currie RF. Risk factors for spontaneous preterm birth among Aboriginal and non-Aboriginal women in Manitoba. Paediatr Perinat Epidemiol. 2005; 19 (3): 181-93.
• ³⁶
  Gilbreath S, Kass PH. Adverse birth outcomes associated with open dumpsites in Alaska Native Villages. Am J Epidemiol. 2006; 164 (6): 518-28.
• ³⁷
  Panaretto K, Lee H, Mitchell M, Larkins S, Manessis V, Buettner P, Watson D. Risk factors for preterm, low birth weight and small for gestational age birth in urban Aboriginal and Torres Strait Islander women in Townsville. Aust N Z J Public Health. 2006; 30 (2): 163-70.
• ³⁸
  Yang M-S, Ho S-Y, Chou F-H, Chang S-J, Ko Y-C. Physical abuse during pregnancy and risk of low-birthweight infants among aborigines in Taiwan. Public Health. 2006; 120 (6): 557-62.
• ³⁹
  Graham S, Pulver LRJ, Wang YA, Kelly PM, Laws PJ, Grayson N, Sulivan EA. The urban-remote divide for Indigenous perinatal outcomes. Med J Aust. 2007; 186 (10): 509-12.
• ⁴⁰
  Simonet F, Wilkins R, Labranche E, Smylie J, Heaman M, Martens P, Fraser WD, Minich K, Wu Y, Carry C, Luo ZC. Primary birthing attendants and birth outcomes in remote Inuit communities - A natural "experiment" in Nunavik, Canada. J Epidemiol Community Health. 2009; 63 (7): 546-51.
• ⁴¹
  Mehaffey K, Higginson A, Cowan J, Osbourne GM, Arbour LT. Maternal smoking at first prenatal visit as a marker of risk for adverse pregnancy outcomes in the Qikiqtaaluk (Baffin) Region. Rural Remote Health. 2010; 10 (3): 1484.
• ⁴²
  Wojtyniak BJ, Rabczenko D, Jönsson BA, Zvezday V, Pedersen HS, Rylander L, Toft G, Ludwicki JK, Góralczyk K, Lesovaya A, Hagmar L, Bonde JP. Association of maternal serum concentrations of 2, 2', 4,4'5,5'-hexa-chlorobiphenyl (CB-153) and 1,1-dichloro-2,2-bis (p-chlorophenyl)-ethylene (p,p'-DDE) levels with birth weight, gestational age and preterm births in Inuit and European populations. Environ Health. 2010; 9 (56): 1-10.
• ⁴³
  Coughlin RL, Kushman EK, Copeland GE, Wilson ML. Pregnancy and birth outcome improvements for American Indians in the Healthy Start project of the Inter-Tribal Council of Michigan, 1998-2008. Matern Child Health J. 2013; 17 (6): 1005-15.
• ⁴⁴
  England LJ, Kim SY, Shapiro-Mendoza CK, Wilson HG, Kendrick JS, Satten GA, Lewis CA, Tucker MJ, Callaghan WM . Effects of maternal smokeless tobacco use on selected pregnancy outcomes in Alaska Native women: a case-control study. Acta Obstet Gynecol Scand. 2013; 92 (6): 648-55.
• ⁴⁵
  Dorfman H, Srinath M, Rockhill K, Hogue C. The Association Between Diabetes Mellitus Among American Indian/Alaska Native Populations with Preterm Birth in Eight US States from 2004-2011. Matern Child Health J. 2015; 19 (11): 2419-28.
• ⁴⁶
  Rothhammer F, Fuentes-Guajardo M, Chakraborty R, Lorenzo Bermejo J, Dittmar M. Neonatal variables, altitude of residence and Aymara ancestry in northern Chile. PLoS One. 2015; 10 (4): e0121834.
• ⁴⁷
  Brown SJ, Mensah FK, Ah Kit J, Stuart-Butler D, Glover K, Leane C, Weetra D, Gartland D, Newbury J, Yelland J. Use of cannabis during pregnancy and birth outcomes in an Aboriginal birth cohort: a cross-sectional, population-based study. BMJ Open. 2016; 6 (2): e010286.
• ⁴⁸
  Oster RT, Toth EL. Longitudinal Rates and Risk Factors for Adverse Birth Weight Among First Nations Pregnancies in Alberta. J. Obstet Gynaecol Can. 2016; 38 (1): 29-34.
• ⁴⁹
  Kildea SV, Gao Y, Rolfe M, Boyle J, Tracy S, Barclay LM. Risk factors for preterm, low birthweight and small for gestational age births among Aboriginal women from remote communities in Northern Australia. Women and Birth. 2017; 30 (5): 398-405.
• ⁵⁰
  Shah PS, Zao J, Al-Wassia H, Shah V. Pregnancy and neonatal outcomes of aboriginal women: a systematic review and meta-analysis. Women's Health Issues. 2011; 21 (1): 28-39.
• ⁵¹
  Oliveira AP, Kalra S, Wahi G, McDonald S, Desai D, Wilson J, Jacobs L, Smoke S, Hill P, Hill K, Kandasamy S, Morrison K, Teo K, Miller R, Anand SS. Maternal and Newborn Health Profile in a First Nations Community in Canada. J. Obstet Gynaecol Can . 2013; 35 (10): 905-13.
• ⁵²
  Marques RP. Um Estudo de Caso Sobre o Fumo, o uso dos cachimbos e as Práticas de Fumar entre os Mbyá - Guarani (RS). Espaço Ameríndio. 2012; 6 (1): 97-118.
• ⁵³
  Santos NL de AC, Costa MCO, Amaral MTR, Vieira GO, Bacelar EB, Almeida AHV. Gravidez na adolescência: análise de fatores de risco para baixo peso, prematuridade e cesariana. Ciênc Saúde Colet. 2014; 19 (3): 719-26.
• ⁵⁴
  Almeida AHV, Costa MCO, Gama SGN da, Amaral MTR, Vieira GO. Baixo peso ao nascer em adolescentes e adultas jovens na Região Nordeste do Brasil. Rev Bras Saúde Mater Infant. 2014; 14 (3): 279-86.
• ⁵⁵
  Smylie J, Firestone M. Back to the basics: Identifying and addressing underlying challenges in achieving high quality and relevant health statistics for indigenous populations in Canada. Stat J IAOS. 2015; 31 (1): 67-87.

Publication Dates

• Publication in this collection
  Jan-Mar 2019

History

• Received
  11 June 2018
• Reviewed
  09 Jan 2019
• Accepted
  25 Jan 2019