Maternal Hookworm Infection and Its Effects on Maternal Health: A Systematic Review and Meta-Analysis

Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and subtropical regions. Pregnancy is an especially vulnerable time for hookworm infection because of its effect on both maternal and subsequently feta...

Full description

Saved in:
Bibliographic Details
Published inThe American journal of tropical medicine and hygiene Vol. 103; no. 5; pp. 1958 - 1968
Main Authors Ness, Tara E, Agrawal, Vedika, Bedard, Kathryn, Ouellette, Lara, Erickson, Timothy A, Hotez, Peter, Weatherhead, Jill E
Format Journal Article
LanguageEnglish
Published United States Institute of Tropical Medicine 01.11.2020
The American Society of Tropical Medicine and Hygiene
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and subtropical regions. Pregnancy is an especially vulnerable time for hookworm infection because of its effect on both maternal and subsequently fetal health. A systematic review and meta-analysis was conducted. The meta-analysis was performed on the association between maternal hookworm and maternal anemia, as well as maternal hookworm coinfection with malaria. The prevalence of hookworm ranged from 1% to 78% in pregnant women, whereas malaria prevalence ranged from 11% to 81%. Pregnant women with hookworm infection were more likely to have anemia (combined odds ratio [cOR] 2.55 [2.20, 2.96], < 0.001). In addition, pregnant woman with hookworm were more likely to have malaria coinfection (cOR 1.60 [1.38, 1.86], < 0.001). Other effects on maternal and child health were investigated and summarized without systematic review or meta-analysis because of the limited study numbers. Despite current deworming recommendations in pregnant women, heavy hookworm burden, coinfection with malaria, and subsequent anemia persist. Although this is likely due, in part, to a lack of implementation of preventive chemotherapy, additional interventions such as health education, proper waste management, or linking malaria and soil-transmitted helminth treatment and prevention programs may also be needed. Further investigations on maternal-child outcomes as a result of hookworm infection during pregnancy will highlight public health interventional targets to reduce morbidity in pregnant women and children globally.
AbstractList Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and subtropical regions. Pregnancy is an especially vulnerable time for hookworm infection because of its effect on both maternal and subsequently fetal health. A systematic review and meta-analysis was conducted. The meta-analysis was performed on the association between maternal hookworm and maternal anemia, as well as maternal hookworm coinfection with malaria. The prevalence of hookworm ranged from 1% to 78% in pregnant women, whereas malaria prevalence ranged from 11% to 81%. Pregnant women with hookworm infection were more likely to have anemia (combined odds ratio [cOR] 2.55 [2.20, 2.96], P < 0.001). In addition, pregnant woman with hookworm were more likely to have malaria coinfection (cOR 1.60 [1.38, 1.86], P < 0.001). Other effects on maternal and child health were investigated and summarized without systematic review or meta-analysis because of the limited study numbers. Despite current deworming recommendations in pregnant women, heavy hookworm burden, coinfection with malaria, and subsequent anemia persist. Although this is likely due, in part, to a lack of implementation of preventive chemotherapy, additional interventions such as health education, proper waste management, or linking malaria and soil-transmitted helminth treatment and prevention programs may also be needed. Further investigations on maternal–child outcomes as a result of hookworm infection during pregnancy will highlight public health interventional targets to reduce morbidity in pregnant women and children globally.
Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and subtropical regions. Pregnancy is an especially vulnerable time for hookworm infection because of its effect on both maternal and subsequently fetal health. A systematic review and meta-analysis was conducted. The meta-analysis was performed on the association between maternal hookworm and maternal anemia, as well as maternal hookworm coinfection with malaria. The prevalence of hookworm ranged from 1% to 78% in pregnant women, whereas malaria prevalence ranged from 11% to 81%. Pregnant women with hookworm infection were more likely to have anemia (combined odds ratio [cOR] 2.55 [2.20, 2.96], P < 0.001). In addition, pregnant woman with hookworm were more likely to have malaria coinfection (cOR 1.60 [1.38, 1.86], P < 0.001). Other effects on maternal and child health were investigated and summarized without systematic review or meta-analysis because of the limited study numbers. Despite current deworming recommendations in pregnant women, heavy hookworm burden, coinfection with malaria, and subsequent anemia persist. Although this is likely due, in part, to a lack of implementation of preventive chemotherapy, additional interventions such as health education, proper waste management, or linking malaria and soil-transmitted helminth treatment and prevention programs may also be needed. Further investigations on maternal–child outcomes as a result of hookworm infection during pregnancy will highlight public health interventional targets to reduce morbidity in pregnant women and children globally.
Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and subtropical regions. Pregnancy is an especially vulnerable time for hookworm infection because of its effect on both maternal and subsequently fetal health. A systematic review and meta-analysis was conducted. The meta-analysis was performed on the association between maternal hookworm and maternal anemia, as well as maternal hookworm coinfection with malaria. The prevalence of hookworm ranged from 1% to 78% in pregnant women, whereas malaria prevalence ranged from 11% to 81%. Pregnant women with hookworm infection were more likely to have anemia (combined odds ratio [cOR] 2.55 [2.20, 2.96], < 0.001). In addition, pregnant woman with hookworm were more likely to have malaria coinfection (cOR 1.60 [1.38, 1.86], < 0.001). Other effects on maternal and child health were investigated and summarized without systematic review or meta-analysis because of the limited study numbers. Despite current deworming recommendations in pregnant women, heavy hookworm burden, coinfection with malaria, and subsequent anemia persist. Although this is likely due, in part, to a lack of implementation of preventive chemotherapy, additional interventions such as health education, proper waste management, or linking malaria and soil-transmitted helminth treatment and prevention programs may also be needed. Further investigations on maternal-child outcomes as a result of hookworm infection during pregnancy will highlight public health interventional targets to reduce morbidity in pregnant women and children globally.
Author Ouellette, Lara
Weatherhead, Jill E
Ness, Tara E
Erickson, Timothy A
Bedard, Kathryn
Hotez, Peter
Agrawal, Vedika
Author_xml – sequence: 1
  givenname: Tara E
  surname: Ness
  fullname: Ness, Tara E
  organization: Department of Pediatrics, Baylor College of Medicine, Houston, Texas
– sequence: 2
  givenname: Vedika
  surname: Agrawal
  fullname: Agrawal, Vedika
  organization: Department of Medicine, Baylor College of Medicine, Houston, Texas
– sequence: 3
  givenname: Kathryn
  surname: Bedard
  fullname: Bedard, Kathryn
  organization: Department of Pediatrics, Baylor College of Medicine, Houston, Texas
– sequence: 4
  givenname: Lara
  surname: Ouellette
  fullname: Ouellette, Lara
  organization: Texas Medical Center Library, Houston, Texas
– sequence: 5
  givenname: Timothy A
  surname: Erickson
  fullname: Erickson, Timothy A
  organization: Department of Pediatrics, Baylor College of Medicine, Houston, Texas
– sequence: 6
  givenname: Peter
  surname: Hotez
  fullname: Hotez, Peter
  organization: Department of Pediatrics, Baylor College of Medicine, Houston, Texas
– sequence: 7
  givenname: Jill E
  surname: Weatherhead
  fullname: Weatherhead, Jill E
  organization: Department of Pediatrics, Baylor College of Medicine, Houston, Texas
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32840198$$D View this record in MEDLINE/PubMed
BookMark eNpdkUFPGzEQha0KVAL02CuyxIXLgsd27N0ekKIoLZFAlUp7thzvLNl016Zrhyj_nt0Aoe1ppDffPM3MOyYHPngk5DOwS8lVcWVXqV1ecpaxMRMfyAikVhkoOT4gI8YYzwol9BE5jnHFGOQc4CM5EjyXDIp8RPDOJuy8behNCL83oWvp3FfoUh08tb6k8xTprBqUSHvpHUfbpOUXOqH325iwtal29Ac-1bjZzd1hstmkJ7exjqfksLJNxE-v9YT8-jr7Ob3Jbr9_m08nt5mT4yJlQi2YW1Qst-AW0Fc1zhW4SqtKaSsUaF5aLXWpclsW2gkEyHNXlpUoFIIWJ-T6xfdxvWixdOhTZxvz2NWt7bYm2Nr82_H10jyEJ6OVVFoNBhevBl34s8aYTFtHh01jPYZ1NFwKDbwAUfTo-X_oKqyH1wyUloL1nqKnshfKdSHGDqv9MsDMEKDZBWg4M0OAPX_29wV7-i0x8Qy2Upmc
CitedBy_id crossref_primary_10_4081_gh_2022_1110
crossref_primary_10_1111_nyas_14985
crossref_primary_10_20961_plexus_v2i4_864
crossref_primary_10_1016_j_ijpara_2021_11_001
crossref_primary_10_1016_j_vaccine_2023_04_025
crossref_primary_10_1016_j_vaccine_2023_05_013
crossref_primary_10_4049_jimmunol_2100708
crossref_primary_10_3389_fimmu_2022_941977
crossref_primary_10_1007_s40475_023_00305_9
crossref_primary_10_3389_ijph_2022_1604620
crossref_primary_10_3390_microorganisms10081591
crossref_primary_10_3889_oamjms_2022_8974
crossref_primary_10_1007_s00436_022_07697_z
crossref_primary_10_3390_ani13121989
Cites_doi 10.1371/journal.pntd.0004566
10.1111/j.1600-0412.2010.01014.x
10.4314/ahs.v18i3.11
10.1186/s12878-018-0096-1
10.1016/j.trstmh.2007.09.015
10.1186/1475-2875-5-99
10.1371/journal.pntd.0000291
10.1186/1471-2458-13-619
10.1371/journal.pntd.0002724
10.1128/CMR.14.4.689-703.2001
10.1007/978-3-030-16061-6_9
10.1186/s40249-017-0307-1
10.1186/s13104-016-2327-5
10.1016/S0140-6736(04)17023-2
10.4269/ajtmh.2007.77.88
10.1186/s12879-016-1413-6
10.1111/j.1365-3156.2010.02598.x
10.4269/ajtmh.2012.12-0371
10.1186/1756-0500-6-263
10.1371/journal.pntd.0005213
10.1136/bmjopen-2016-011458
10.7897/2230-8407.0510151
10.1371/journal.pone.0188783
10.1186/1756-3305-5-296
10.1371/journal.pone.0186724
10.1186/s40794-019-0088-6
10.1371/journal.pntd.0003466
10.1093/trstmh/trt086
10.4269/ajtmh.2011.10-0186
10.1111/j.1753-4887.2011.00437.x
10.1016/j.vaccine.2016.03.018
10.1371/journal.pntd.0006269
10.4269/ajtmh.2009.80.896
10.1371/journal.pone.0206880
10.1155/2014/108593
10.1111/j.1365-3016.1990.tb00638.x
10.1371/journal.pntd.0006940
10.1111/j.1365-3156.2006.01706.x
10.1055/s-2000-9508
10.1371/journal.pntd.0004922
10.2147/IJWH.S103529
10.1093/trstmh/trx082
10.1371/journal.pntd.0000270
10.1016/j.ijpara.2019.02.005
10.4269/ajtmh.2010.09-0165
10.1196/annals.1425.000
10.1186/s12879-019-4135-8
10.1097/COH.0b013e3283524d90
10.1111/j.1365-3016.2012.01280.x
10.1086/591183
10.1371/journal.pntd.0007406
10.1016/j.preghy.2018.06.001
10.1097/QAI.0b013e3182511e42
10.1093/cid/ciu715
10.1371/journal.pntd.0000370
10.1038/sj.ejcn.1602812
10.1371/journal.pntd.0004397
10.1093/ajcn/71.5.1280s
10.1016/S0140-6736(18)32279-7
10.1371/journal.pntd.0000887
10.1186/s13104-017-2770-y
10.1371/journal.pntd.0003463
10.1016/j.vaccine.2010.10.047
10.1111/1471-0528.15585
10.1186/s12884-018-1739-8
10.3109/00016349309068032
10.4269/ajtmh.17-0934
10.1016/S0035-9203(01)90164-6
10.1371/journal.pntd.0000473
10.1017/S1368980014001888
ContentType Journal Article
Copyright Copyright Institute of Tropical Medicine Nov 2020
The American Society of Tropical Medicine and Hygiene 2020
Copyright_xml – notice: Copyright Institute of Tropical Medicine Nov 2020
– notice: The American Society of Tropical Medicine and Hygiene 2020
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
5PM
DOI 10.4269/ajtmh.20-0503
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList

MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
Public Health
EISSN 1476-1645
EndPage 1968
ExternalDocumentID 10_4269_ajtmh_20_0503
32840198
Genre Meta-Analysis
Systematic Review
Journal Article
GrantInformation_xml – fundername: NIAID NIH HHS
  grantid: K08 AI143968
GroupedDBID ---
.55
.GJ
1CY
23M
2WC
34G
36B
3O-
53G
5GY
5RE
5VS
6J9
ABCQX
ABPPZ
ABTNK
ACGFO
ADBBV
ADTPD
AENEX
AFFNX
AGCDD
AI.
AIAGR
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BTFSW
CGR
CUY
CVF
DIK
E3Z
EBD
EBS
ECM
EIF
EJD
EMB
EMOBN
F5P
GX1
H13
HYE
K-O
KQ8
L7B
MV1
NEJ
NPM
OHT
OK1
P2P
PQQKQ
RHF
RHI
RPM
SV3
TR2
TST
UPT
VH1
W8F
WH7
WOQ
WOW
X7M
XOL
ZGI
ZKB
ZXP
~KM
AAYXX
CITATION
7X8
5PM
ID FETCH-LOGICAL-c459t-36b0cbf08a1cb1f0865861cf76f67a36172da747d68ad97c3e1188cddf396e173
IEDL.DBID RPM
ISSN 0002-9637
IngestDate Tue Sep 17 21:28:42 EDT 2024
Sat Aug 17 00:14:31 EDT 2024
Thu Oct 10 16:33:32 EDT 2024
Fri Dec 06 04:24:28 EST 2024
Sat Sep 28 08:27:09 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 5
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c459t-36b0cbf08a1cb1f0865861cf76f67a36172da747d68ad97c3e1188cddf396e173
Notes ObjectType-Article-2
SourceType-Scholarly Journals-1
ObjectType-Feature-1
content type line 23
ObjectType-Undefined-3
Disclosure: P. H. is a patent holder and lead investigator on vaccines against hookworm both in clinical trials and in development.
Authors’ addresses: Tara E. Ness, Vedika Agrawal, Kathryn Bedard, and Jill E. Weatherhead, Department of Pediatrics, Baylor College of Medicine, Houston, TX, E-mails: tara.ness@bcm.edu, vedika.agrawal@bcm.edu, kathryn.bedard@bcm.edu, and weatherh@bcm.edu. Lara Ouellette, Texas Medical Center Library, Liaison, Houston, TX, E-mail: lara.ouellette@library.tmc.edu. Timothy A. Erickson, Department of Pediatrics, Baylor College of Medicine, Section of Pediatric Tropical Medicine, Houston, TX, E-mail: timothy.erickson@bcm.edu. Peter Hotez, Department of Pediatrics, Baylor College of Medicine, Houston, TX, and Department of Pediatrics, Texas Children’s Hospital, Houston, TX, E-mail: hotez@bcm.edu.
OpenAccessLink https://www.ajtmh.org/downloadpdf/journals/tpmd/103/5/article-p1958.pdf
PMID 32840198
PQID 2474307643
PQPubID 105381
PageCount 11
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_7646767
proquest_miscellaneous_2437129139
proquest_journals_2474307643
crossref_primary_10_4269_ajtmh_20_0503
pubmed_primary_32840198
PublicationCentury 2000
PublicationDate 2020-11-01
PublicationDateYYYYMMDD 2020-11-01
PublicationDate_xml – month: 11
  year: 2020
  text: 2020-11-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: Deerfield, Illinois
PublicationTitle The American journal of tropical medicine and hygiene
PublicationTitleAlternate Am J Trop Med Hyg
PublicationYear 2020
Publisher Institute of Tropical Medicine
The American Society of Tropical Medicine and Hygiene
Publisher_xml – name: Institute of Tropical Medicine
– name: The American Society of Tropical Medicine and Hygiene
References Fairley (b66) 2013; 88
Salam (b23) 2015; 6
Blackwell (b16) 2016; 8
Hotez (b87) 2008; 2
Melku (b49) 2014; 2014
Ekejindu (b39) 2011; 6
Feleke (b41) 2018; 18
McClure (b67) 2014; 8
Makhoul (b32) 2012; 43
Gyorkos (b10) 2019; 49
Fuseini (b25) 2010; 2
Bartsch (b2) 2016; 10
Adegnika (b15) 2012; 7
Chen (b79) 2018; 13
Yatich (b65) 2010; 82
Phuanukoonnon (b52) 2013; 56
Getachew (b43) 2013; 6
(b12) 2016
Imhoff-Kunsch (b19) 2012; 26
Ojurongbe (b51) 2018; 18
Montresor (b76) 2017; 111
Torlesse (b73) 2001; 95
Aikawa (b28) 2008; 62
Khambalia (b20) 2011; 69
Gyorkos (b44) 2010; 83
Haider (b18) 2009; 2
Thayer (b24) 2017; 97
González-Fernández (b59) 2017; 6
Malhotra (b62) 2015; 9
Allen (b81) 2000; 71
Ebuy (b29) 2017; 12
Mireku (b68) 2015; 9
Ndyomugyenyi (b33) 2008; 102
(b9) 2002
Mupfasoni (b69) 2018; 12
Majid (b4) 2019; 13
(b1) 2018; 392
Bolka (b38) 2019; 19
Agu (b27) 2013; 14
Colomer (b84) 1990; 4
Xiong (b80) 2000; 17
Mengist (b50) 2017; 10
Kizito (b63) 2013; 13
Lin (b83) 2018; 18
Parks (b78) 2019; 126
Fairley (b40) 2010; 83
Hotez (b88) 2019
Boel (b37) 2010; 4
Elliott (b64) 2010; 29
Hotez (b7) 2018; 98
(b77) 2018
Urassa (b74) 2011; 8
Thi Tran (b53) 2019; 14
Bangert (b70) 2019; 13
Yatich (b56) 2009; 80
Larocque (b72) 2006; 11
Adegnika (b35) 2010; 15
Kumera (b47) 2018; 13
Webb (b58) 2012; 60
Brooker (b86) 2006; 5
Roberts (b22) 2011; 1
Loukas (b60) 2001; 14
Ababiya (b14) 2014; 5
Naing (b21) 2013; 107
Getachew (b42) 2012; 5
Woodburn (b57) 2009; 3
Mahande (b31) 2016; 16
Brooker (b85) 2007; 77
Bartsch (b89) 2016; 34
Mutuku (b26) 2014; 91
Downes (b13) 2016; 6
Lebso (b48) 2017; 12
Rasmussen (b82) 1993; 72
Campbell (b17) 2016; 10
(b3) 2013
Lenk (b5) 2016; 10
Hailu (b45) 2019; 5
Hotez (b6) 2008; 1136
Ivan (b71) 2014; 60
Brooker (b8) 2008; 2
Lindström (b30) 2011; 90
Christian (b75) 2004; 364
Van Eijk (b55) 2009; 3
Tay (b34) 2017; 10
Hillier (b46) 2008; 198
Nash (b61) 2017; 11
Baingana (b36) 2015; 18
Thigpen (b54) 2011; 84
(b11) 2017
References_xml – volume: 10
  start-page: e0004566
  year: 2016
  ident: b17
  article-title: Complexities and perplexities: a critical appraisal of the evidence for soil-transmitted helminth infection-related morbidity
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0004566
  contributor:
    fullname: Campbell
– volume: 90
  start-page: 47
  year: 2011
  ident: b30
  article-title: Prevalence of anemia and micronutrient deficiencies in early pregnancy in rural Bangladesh, the MINIMat trial
  publication-title: Acta Obstet Gynecol Scand
  doi: 10.1111/j.1600-0412.2010.01014.x
  contributor:
    fullname: Lindström
– volume: 18
  start-page: 542
  year: 2018
  ident: b51
  article-title: Prevalence and associated factors of Plasmodium falciparum and soil transmitted helminth infections among pregnant women in Osun state, Nigeria
  publication-title: Afr Health Sci
  doi: 10.4314/ahs.v18i3.11
  contributor:
    fullname: Ojurongbe
– volume: 18
  start-page: 2
  year: 2018
  ident: b41
  article-title: Pregnant mothers are more anemic than lactating mothers, a comparative cross-sectional study, Bahir Dar, Ethiopia
  publication-title: BMC Hematol
  doi: 10.1186/s12878-018-0096-1
  contributor:
    fullname: Feleke
– volume: 102
  start-page: 130
  year: 2008
  ident: b33
  article-title: Malaria and hookworm infections in relation to haemoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda
  publication-title: Trans R Soc Trop Med Hyg
  doi: 10.1016/j.trstmh.2007.09.015
  contributor:
    fullname: Ndyomugyenyi
– volume: 5
  start-page: 99
  year: 2006
  ident: b86
  article-title: The co-distribution of Plasmodium falciparum and hookworm among African schoolchildren
  publication-title: Malar J
  doi: 10.1186/1475-2875-5-99
  contributor:
    fullname: Brooker
– volume: 2
  start-page: e291
  year: 2008
  ident: b8
  article-title: Hookworm-related anaemia among pregnant women: a systematic review
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0000291
  contributor:
    fullname: Brooker
– volume: 6
  start-page: CD005547
  year: 2015
  ident: b23
  article-title: Effect of administration of antihelminthics for soil-transmitted helminths during pregnancy
  publication-title: Cochrane Database Syst Rev
  contributor:
    fullname: Salam
– volume: 13
  start-page: 619
  year: 2013
  ident: b63
  article-title: Factors affecting the infant antibody response to measles immunisation in Entebbe-Uganda
  publication-title: BMC Public Health
  doi: 10.1186/1471-2458-13-619
  contributor:
    fullname: Kizito
– volume: 14
  start-page: 180
  year: 2019
  ident: b53
  article-title: Soil-transmitted helminth infection and its association with anemia and zinc deficiency among women in Nghe An Province, Vietnam
  publication-title: Iranian J Parasitol
  contributor:
    fullname: Thi Tran
– volume: 8
  start-page: e2724
  year: 2014
  ident: b67
  article-title: The association of parasitic infections in pregnancy and maternal and fetal anemia: a cohort study in coastal Kenya
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0002724
  contributor:
    fullname: McClure
– volume: 14
  start-page: 689
  year: 2001
  ident: b60
  article-title: Immune responses in hookworm infections
  publication-title: Clin Microbiol Rev
  doi: 10.1128/CMR.14.4.689-703.2001
  contributor:
    fullname: Loukas
– start-page: 75
  volume-title: Curious 2018: Future Insights in Science and Technology
  year: 2019
  ident: b88
  article-title: Neglected parasitic infections and the syndemic anemia vaccines for Africa
  doi: 10.1007/978-3-030-16061-6_9
  contributor:
    fullname: Hotez
– volume: 6
  start-page: 94
  year: 2017
  ident: b59
  article-title: C-reactive protein is differentially modulated by co-existing infections, vitamin deficiencies and maternal factors in pregnant and lactating indigenous Panamanian women
  publication-title: Infect Dis Poverty
  doi: 10.1186/s40249-017-0307-1
  contributor:
    fullname: González-Fernández
– volume: 10
  start-page: 3
  year: 2017
  ident: b34
  article-title: Parasitic infections and maternal anaemia among expectant mothers in the Dangme East District of Ghana
  publication-title: BMC Res Notes
  doi: 10.1186/s13104-016-2327-5
  contributor:
    fullname: Tay
– volume: 364
  start-page: 981
  year: 2004
  ident: b75
  article-title: Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal
  publication-title: Lancet
  doi: 10.1016/S0140-6736(04)17023-2
  contributor:
    fullname: Christian
– volume: 77
  start-page: 88
  year: 2007
  ident: b85
  article-title: Epidemiology of plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control
  publication-title: A J Trop Med Hyg
  doi: 10.4269/ajtmh.2007.77.88
  contributor:
    fullname: Brooker
– volume: 16
  start-page: 78
  year: 2016
  ident: b31
  article-title: Prevalence of parasitic infections and associations with pregnancy complications and outcomes in northern Tanzania: a registry-based cross-sectional study
  publication-title: BMC Infect Dis
  doi: 10.1186/s12879-016-1413-6
  contributor:
    fullname: Mahande
– volume: 15
  start-page: 1204
  year: 2010
  ident: b35
  article-title: Epidemiology of parasitic co‐infections during pregnancy in Lambaréné
  publication-title: Gabon Trop Med Int Health
  doi: 10.1111/j.1365-3156.2010.02598.x
  contributor:
    fullname: Adegnika
– volume: 88
  start-page: 48
  year: 2013
  ident: b66
  article-title: Birthweight in offspring of mothers with high prevalence of helminth and malaria infection in coastal Kenya
  publication-title: Am J Trop Med Hyg
  doi: 10.4269/ajtmh.2012.12-0371
  contributor:
    fullname: Fairley
– volume: 6
  start-page: 263
  year: 2013
  ident: b43
  article-title: Prevalence soil transmitted helminthiasis and malaria co-infection among pregnant women and risk factors in Gilgel Gibe dam Area, Southwest Ethiopia
  publication-title: BMC Res Notes
  doi: 10.1186/1756-0500-6-263
  contributor:
    fullname: Getachew
– volume: 11
  start-page: e0005213
  year: 2017
  ident: b61
  article-title: The impact of prenatal exposure to parasitic infections and to anthelminthic treatment on antibody responses to routine immunisations given in infancy: secondary analysis of a randomised controlled trial
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0005213
  contributor:
    fullname: Nash
– volume: 6
  start-page: e011458
  year: 2016
  ident: b13
  article-title: Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS)
  publication-title: BMJ Open
  doi: 10.1136/bmjopen-2016-011458
  contributor:
    fullname: Downes
– volume: 83
  start-page: 354
  year: 2010
  ident: b44
  article-title: Hookworm and Trichuris infections associated with anemia during pregnancy
  publication-title: Am J Trop Med Hyg
  contributor:
    fullname: Gyorkos
– volume: 5
  start-page: 737
  year: 2014
  ident: b14
  article-title: Prevalence of anemia among pregnant women in Ethiopia and its management: a review
  publication-title: Int Res J Pharm
  doi: 10.7897/2230-8407.0510151
  contributor:
    fullname: Ababiya
– volume: 12
  start-page: e0188783
  year: 2017
  ident: b48
  article-title: Prevalence of anemia and associated factors among pregnant women in Southern Ethiopia: a community based cross-sectional study
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0188783
  contributor:
    fullname: Lebso
– volume: 5
  start-page: 296
  year: 2012
  ident: b42
  article-title: Anaemia and associated risk factors among pregnant women in Gilgel Gibe dam area, Southwest Ethiopia
  publication-title: Parasit Vectors
  doi: 10.1186/1756-3305-5-296
  contributor:
    fullname: Getachew
– volume: 12
  start-page: e0186724
  year: 2017
  ident: b29
  article-title: Determinants of severe anemia among laboring mothers in Mekelle city public hospitals, Tigray region, Ethiopia
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0186724
  contributor:
    fullname: Ebuy
– volume-title: Report of a WHO Expert Committee
  year: 2002
  ident: b9
  article-title: Prevention and control of schistosomiasis and soil-transmitted helminthiasis
– volume: 5
  start-page: 13
  year: 2019
  ident: b45
  article-title: Determinant factors of anaemia among pregnant women attending antenatal care clinic in Northwest Ethiopia
  publication-title: Trop Dis Travel Med Vaccines
  doi: 10.1186/s40794-019-0088-6
  contributor:
    fullname: Hailu
– volume: 9
  start-page: e0003466
  year: 2015
  ident: b62
  article-title: Effect of antenatal parasitic infections on anti-vaccine IgG levels in children: a prospective birth cohort study in Kenya
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0003466
  contributor:
    fullname: Malhotra
– volume: 107
  start-page: 672
  year: 2013
  ident: b21
  article-title: Malaria and soil-transmitted intestinal helminth co-infection and its effect on anemia: a meta-analysis
  publication-title: Trans R Soc Trop Med Hyg
  doi: 10.1093/trstmh/trt086
  contributor:
    fullname: Naing
– volume: 84
  start-page: 379
  year: 2011
  ident: b54
  article-title: Associations between peripheral Plasmodium falciparum malaria parasitemia, human immunodeficiency virus, and concurrent helminthic infection among pregnant women in Malawi
  publication-title: Am J Trop Med Hyg
  doi: 10.4269/ajtmh.2011.10-0186
  contributor:
    fullname: Thigpen
– volume: 69
  start-page: 693
  year: 2011
  ident: b20
  article-title: Burden of anemia among indigenous populations
  publication-title: Nutr Rev
  doi: 10.1111/j.1753-4887.2011.00437.x
  contributor:
    fullname: Khambalia
– volume: 34
  start-page: 2197
  year: 2016
  ident: b89
  article-title: Modeling the economic and epidemiologic impact of hookworm vaccine and mass drug administration (MDA) in Brazil, a high transmission setting
  publication-title: Vaccine
  doi: 10.1016/j.vaccine.2016.03.018
  contributor:
    fullname: Bartsch
– volume: 91
  start-page: 329
  year: 2014
  ident: b26
  article-title: Marked changes in maternal parasitic infections in Kwale county (2006–2014)
  publication-title: Am J Trop Med Hyg
  contributor:
    fullname: Mutuku
– volume: 1
  start-page: 189
  year: 2011
  ident: b22
  article-title: Epidemiology and aetiology of maternal parasitic infections in low- and middle-income countries
  publication-title: J Glob Health
  contributor:
    fullname: Roberts
– volume: 12
  start-page: e0006269
  year: 2018
  ident: b69
  article-title: Estimation of the number of women of reproductive age in need of preventive chemotherapy for soil-transmitted helminth infections
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0006269
  contributor:
    fullname: Mupfasoni
– volume: 80
  start-page: 896
  year: 2009
  ident: b56
  article-title: Malaria and intestinal helminth co-infection among pregnant women in Ghana: prevalence and risk factors
  publication-title: Am J Trop Med Hyg
  doi: 10.4269/ajtmh.2009.80.896
  contributor:
    fullname: Yatich
– volume: 13
  start-page: e0206880
  year: 2018
  ident: b47
  article-title: Anemia and its association with coffee consumption and hookworm infection among pregnant women attending antenatal care at Debre Markos Referral Hospital, Northwest Ethiopia
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0206880
  contributor:
    fullname: Kumera
– volume: 2014
  start-page: 108593
  year: 2014
  ident: b49
  article-title: Prevalence and predictors of maternal anemia during pregnancy in Gondar, Northwest Ethiopia: an institutional based cross-sectional study
  publication-title: Anemia
  doi: 10.1155/2014/108593
  contributor:
    fullname: Melku
– volume: 4
  start-page: 196
  year: 1990
  ident: b84
  article-title: Anaemia during pregnancy as a risk factor for infant iron deficiency: report from the Valencia Infant Anaemia Cohort (VIAC) study
  publication-title: Paediatr Perinat Epidemiol
  doi: 10.1111/j.1365-3016.1990.tb00638.x
  contributor:
    fullname: Colomer
– volume: 8
  start-page: 176
  year: 2011
  ident: b74
  article-title: Effectiveness of routine antihelminthic treatment on anaemia in pregnancy in Rufiji District, Tanzania: a cluster randomised controlled trial
  publication-title: East Afr J Public Health
  contributor:
    fullname: Urassa
– volume-title: WHO Recommendations on Antenatal Care for a Positive Pregnancy Experience
  year: 2016
  ident: b12
– volume: 13
  start-page: e0006940
  year: 2019
  ident: b4
  article-title: Resolving “worm wars”: an extended comparison review of findings from key economics and epidemiological studies
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0006940
  contributor:
    fullname: Majid
– volume: 11
  start-page: 1485
  year: 2006
  ident: b72
  article-title: A double‐blind randomized controlled trial of antenatal mebendazole to reduce low birthweight in a hookworm‐endemic area of Peru
  publication-title: Trop Med Int Health
  doi: 10.1111/j.1365-3156.2006.01706.x
  contributor:
    fullname: Larocque
– volume-title: Reaching Girls and Women of Reproductive Age with Deworming: Report of the Advisory Group on Deworming in Girls and Women of Reproductive Age
  year: 2018
  ident: b77
– volume: 17
  start-page: 137
  year: 2000
  ident: b80
  article-title: Anemia during pregnancy and birth outcome: a meta-analysis
  publication-title: Am J Perinatol
  doi: 10.1055/s-2000-9508
  contributor:
    fullname: Xiong
– volume: 10
  start-page: e0004922
  year: 2016
  ident: b2
  article-title: The global economic and health burden of human hookworm infection
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0004922
  contributor:
    fullname: Bartsch
– volume: 8
  start-page: 651
  year: 2016
  ident: b16
  article-title: Helminth infection during pregnancy: insights from evolutionary ecology
  publication-title: Int J Womens Health
  doi: 10.2147/IJWH.S103529
  contributor:
    fullname: Blackwell
– volume: 43
  start-page: 735
  year: 2012
  ident: b32
  article-title: Risk factors associated with anemia, iron deficiency and iron deficiency anemia in rural Nepali pregnant women
  publication-title: Southeast Asian J Trop Med Public Health
  contributor:
    fullname: Makhoul
– volume: 2
  start-page: CD005547
  year: 2009
  ident: b18
  article-title: Effect of administration of antihelminthics for soil transmitted helminths during pregnancy
  publication-title: Cochrane Database Syst Rev
  contributor:
    fullname: Haider
– volume: 111
  start-page: 457
  year: 2017
  ident: b76
  article-title: Preventive chemotherapy to control soil-transmitted helminthiasis averted more than 500 000 DALYs in 2015
  publication-title: Trans R Soc Trop Med Hyg
  doi: 10.1093/trstmh/trx082
  contributor:
    fullname: Montresor
– volume: 2
  start-page: e270
  year: 2008
  ident: b87
  article-title: Tropical anemia: one of Africa’s great killers and a rationale for linking malaria and neglected tropical disease control to achieve a common goal
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0000270
  contributor:
    fullname: Hotez
– volume: 49
  start-page: 541
  year: 2019
  ident: b10
  article-title: Systematic review of exposure to albendazole or mebendazole during pregnancy and effects on maternal and child outcomes, with particular reference to exposure in the first trimester
  publication-title: Int J Parasitol
  doi: 10.1016/j.ijpara.2019.02.005
  contributor:
    fullname: Gyorkos
– volume: 56
  start-page: 119
  year: 2013
  ident: b52
  article-title: Intestinal parasitic infections and anaemia among pregnant women in the highlands of Papua New Guinea
  publication-title: Papua New Guinea Med J
  contributor:
    fullname: Phuanukoonnon
– volume: 82
  start-page: 28
  year: 2010
  ident: b65
  article-title: The effect of malaria and intestinal helminth coinfection on birth outcomes in Kumasi, Ghana
  publication-title: Am J Trop Med Hyg
  doi: 10.4269/ajtmh.2010.09-0165
  contributor:
    fullname: Yatich
– volume: 1136
  start-page: 38
  year: 2008
  ident: b6
  article-title: Hookworm and poverty
  publication-title: Ann N Y Acad Sci
  doi: 10.1196/annals.1425.000
  contributor:
    fullname: Hotez
– volume-title: Parasites-Hookworm
  year: 2013
  ident: b3
– volume: 19
  start-page: 483
  year: 2019
  ident: b38
  article-title: Prevalence of intestinal parasitic infection and its association with anemia among pregnant women in Wondo Genet district, Southern Ethiopia: a cross-sectional study
  publication-title: BMC Infect Dis
  doi: 10.1186/s12879-019-4135-8
  contributor:
    fullname: Bolka
– volume-title: Preventive Chemotherapy to Control Soil-Transmitted Helminth Infections in at-Risk Population Groups
  year: 2017
  ident: b11
– volume: 7
  start-page: 221
  year: 2012
  ident: b15
  article-title: Epidemiology of malaria and helminth interaction: a review from 2001 to 2011
  publication-title: Curr Opin HIV AIDS
  doi: 10.1097/COH.0b013e3283524d90
  contributor:
    fullname: Adegnika
– volume: 26
  start-page: 223
  year: 2012
  ident: b19
  article-title: Antihelminthics in pregnancy and maternal, newborn and child health
  publication-title: Paediatr Perinat Epidemiol
  doi: 10.1111/j.1365-3016.2012.01280.x
  contributor:
    fullname: Imhoff-Kunsch
– volume: 198
  start-page: 920
  year: 2008
  ident: b46
  article-title: Plasmodium falciparum and helminth coinfection in a semiurban population of pregnant women in Uganda
  publication-title: J Infect Dis
  doi: 10.1086/591183
  contributor:
    fullname: Hillier
– volume: 13
  start-page: e0007406
  year: 2019
  ident: b70
  article-title: Provision of deworming intervention to pregnant women by antenatal services in countries endemic for soil-transmitted helminthiasis
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0007406
  contributor:
    fullname: Bangert
– volume: 13
  start-page: 141
  year: 2018
  ident: b79
  article-title: Severe anemia, sickle cell disease, and thalassemia as risk factors for hypertensive disorders in pregnancy in developing countries
  publication-title: Pregnancy Hypertens
  doi: 10.1016/j.preghy.2018.06.001
  contributor:
    fullname: Chen
– volume: 60
  start-page: 307
  year: 2012
  ident: b58
  article-title: The effect of anthelminthic treatment during pregnancy on HIV plasma viral load; results from a randomised, double blinded, placebo-controlled trial in Uganda
  publication-title: J Acquir Immune Defici Syndr
  doi: 10.1097/QAI.0b013e3182511e42
  contributor:
    fullname: Webb
– volume: 60
  start-page: 135
  year: 2014
  ident: b71
  article-title: Effect of deworming on disease progression markers in HIV-1–Infected pregnant women on antiretroviral therapy: a longitudinal observational study from Rwanda
  publication-title: Clin Infect Dis
  doi: 10.1093/cid/ciu715
  contributor:
    fullname: Ivan
– volume: 3
  start-page: e370
  year: 2009
  ident: b55
  article-title: Geohelminth infections among pregnant women in rural western Kenya; a cross-sectional study
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0000370
  contributor:
    fullname: Van Eijk
– volume: 14
  start-page: 27
  year: 2013
  ident: b27
  article-title: Impact of Plasmodium falciparum and hookworm infections on the frequency of anaemia in pregnant women of rural communities in Enugu, South East Nigeria
  publication-title: Pan Afr Med J
  contributor:
    fullname: Agu
– volume: 62
  start-page: 946
  year: 2008
  ident: b28
  article-title: Prenatal iron supplementation in rural Vietnam
  publication-title: Eur J Clin Nutr
  doi: 10.1038/sj.ejcn.1602812
  contributor:
    fullname: Aikawa
– volume: 10
  start-page: e0004397
  year: 2016
  ident: b5
  article-title: Productivity loss related to neglected tropical diseases eligible for preventive chemotherapy: a systematic literature review
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0004397
  contributor:
    fullname: Lenk
– volume: 2
  start-page: 48
  year: 2010
  ident: b25
  article-title: Parasitic infections and anaemia during pregnancy in the Kassena-Nankana district of Northern Ghana
  publication-title: J Public Health Epidemiol
  contributor:
    fullname: Fuseini
– volume: 71
  start-page: 1280S
  year: 2000
  ident: b81
  article-title: Anemia and iron deficiency: effects on pregnancy outcome
  publication-title: Am J Clin Nutr
  doi: 10.1093/ajcn/71.5.1280s
  contributor:
    fullname: Allen
– volume: 392
  start-page: 1789
  year: 2018
  ident: b1
  article-title: Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017
  publication-title: Lancet
  doi: 10.1016/S0140-6736(18)32279-7
– volume: 83
  start-page: 147
  year: 2010
  ident: b40
  article-title: The effects of maternal helminth infection and co-infection with malaria on birthweight and subsequent growth in offspring in a population on the coast of Kenya
  publication-title: Am J Trop Med Hyg
  contributor:
    fullname: Fairley
– volume: 4
  start-page: e887
  year: 2010
  ident: b37
  article-title: Complex interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0000887
  contributor:
    fullname: Boel
– volume: 10
  start-page: 440
  year: 2017
  ident: b50
  article-title: Intestinal helminthic infection and anemia among pregnant women attending ante-natal care (ANC) in East Wollega, Oromia, Ethiopia
  publication-title: BMC Res Notes
  doi: 10.1186/s13104-017-2770-y
  contributor:
    fullname: Mengist
– volume: 9
  start-page: e0003463
  year: 2015
  ident: b68
  article-title: Impact of helminth infection during pregnancy on cognitive and motor functions of one-year-old children
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0003463
  contributor:
    fullname: Mireku
– volume: 29
  start-page: 247
  year: 2010
  ident: b64
  article-title: Effects of maternal and infant co-infections, and of maternal immunisation, on the infant response to BCG and tetanus immunisation
  publication-title: Vaccine
  doi: 10.1016/j.vaccine.2010.10.047
  contributor:
    fullname: Elliott
– volume: 6
  start-page: 33
  year: 2011
  ident: b39
  article-title: Malaria and hookworm co-infection among pregnant and non-pregnant women in a semi-urban area in Anambra State, Nigeria
  publication-title: World J Med Sci
  contributor:
    fullname: Ekejindu
– volume: 97
  start-page: 470
  year: 2017
  ident: b24
  article-title: Effects of deworming on maternal and child health: a literature review and meta-analysis for the lives saved tool
  publication-title: Am J Trop Med Hyg
  contributor:
    fullname: Thayer
– volume: 126
  start-page: 737
  year: 2019
  ident: b78
  article-title: Maternal anaemia and maternal, fetal, and neonatal outcomes in a prospective cohort study in India and Pakistan
  publication-title: BJOG
  doi: 10.1111/1471-0528.15585
  contributor:
    fullname: Parks
– volume: 18
  start-page: 111
  year: 2018
  ident: b83
  article-title: Prevalence, risk factors and associated adverse pregnancy outcomes of anaemia in Chinese pregnant women: a multicentre retrospective study
  publication-title: BMC Pregnancy Childbirth
  doi: 10.1186/s12884-018-1739-8
  contributor:
    fullname: Lin
– volume: 72
  start-page: 246
  year: 1993
  ident: b82
  article-title: First-and second-trimester hemoglobin levels: relation to birth weight and gestational age
  publication-title: Acta obstetricia gynecologica Scand
  doi: 10.3109/00016349309068032
  contributor:
    fullname: Rasmussen
– volume: 98
  start-page: 1211
  year: 2018
  ident: b7
  article-title: Empowering girls and women through hookworm prevention
  publication-title: Am J Trop Med Hyg
  doi: 10.4269/ajtmh.17-0934
  contributor:
    fullname: Hotez
– volume: 95
  start-page: 195
  year: 2001
  ident: b73
  article-title: Albendazole therapy and reduced decline in haemoglobin concentration during pregnancy (Sierra Leone)
  publication-title: Trans R Soc Trop Med Hyg
  doi: 10.1016/S0035-9203(01)90164-6
  contributor:
    fullname: Torlesse
– volume: 3
  start-page: e473
  year: 2009
  ident: b57
  article-title: Risk factors for helminth, malaria, and HIV infection in pregnancy in Entebbe, Uganda
  publication-title: PLoS Negl Trop Dis
  doi: 10.1371/journal.pntd.0000473
  contributor:
    fullname: Woodburn
– volume: 18
  start-page: 1423
  year: 2015
  ident: b36
  article-title: The aetiology of anaemia during pregnancy: a study to evaluate the contribution of iron deficiency and common infections in pregnant Ugandan women
  publication-title: Public Health Nutr
  doi: 10.1017/S1368980014001888
  contributor:
    fullname: Baingana
SSID ssj0018211
Score 2.4318283
SecondaryResourceType review_article
Snippet Hookworm is an intestinal parasite that infects nearly 230 million people, with another 5.1 billion at risk, especially in poverty-stricken tropical and...
SourceID pubmedcentral
proquest
crossref
pubmed
SourceType Open Access Repository
Aggregation Database
Index Database
StartPage 1958
SubjectTerms Ancylostomatoidea
Anemia
Anemia - complications
Anemia - epidemiology
Anemia - parasitology
Animals
Cohort Studies
Coinfection
Cross-Sectional Studies
Female
Health Education
Hookworm Infections - complications
Hookworm Infections - epidemiology
Hookworm Infections - parasitology
Humans
Infections
Malaria
Malaria - complications
Malaria - epidemiology
Malaria - parasitology
Maternal & child health
Maternal Health
Meta-analysis
Pregnancy
Pregnancy Complications, Parasitic - epidemiology
Pregnancy Complications, Parasitic - parasitology
Public Health
Systematic review
Womens health
Title Maternal Hookworm Infection and Its Effects on Maternal Health: A Systematic Review and Meta-Analysis
URI https://www.ncbi.nlm.nih.gov/pubmed/32840198
https://www.proquest.com/docview/2474307643
https://search.proquest.com/docview/2437129139
https://pubmed.ncbi.nlm.nih.gov/PMC7646767
Volume 103
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3PS8MwFH5sHsSL-NvpHBHEW1zSdknmTUSdQkVQYbeSpikqrorr8N_3JW2n05unQJPQ8t5L8z2-ly8AR1JnTgAgoENmMhoZKWlqmKE84lGAc5j1l03Et2L0GN2MB-MWDJqzML5o36TPJ8Xr5KR4fvK1le8T02_qxPp38bkUkdMZ67ehjdtvk6LX1IEKOG8wL0aXrIQ13YnNvn4pJ46AoE4EZQWWQ_w3I8RRi3vSH6D5u17yxwZ0uQarNXIkZ9UXrkPLFhuwHNfc-CbYWFeCzmSEwPkTsSi5riutCqKLjFyXU1KJFU8JPvoe7kvATskZuZ_LOpOKM_DzYltq2oiXbMHj5cXD-YjWlyhQEw2GJQ1FykyaM6W5STm2CDkEN7kUuZA6dAAm05hTZELpbChNiM5RymRZHg6F5TLchqXirbC7QJRwPCniqVxho3JlHZ2sghxzHiYD1oHjxozJe6WVkWCO4UyfeNMnAUuc6TvQbYyc1EtmmgQRghmGrsXuw3k3BrtjMHRh32ZuTCgRoCBq7cBO5ZP5mxpndkAueGs-wAlpL_ZgfHlB7Tqe9v49cx9WApeH-zOKXVgqP2b2AMFKmfagfTXmPR-iX4VK6YA
link.rule.ids 230,314,727,780,784,885,27924,27925,53791,53793
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1RT9swED4Bk0pfJgaDdYPNkxBvpnaS2g5vqAK1g6BJgMRb5DiOKFrTiqbi7-_sJIWOtz1Zim0lujvH3-k7fwY4ljp3AgABjZnJaWSkpJlhhvKIRwHOYdZfNpHciNF99Oth8LABg_YsjC_aN9nktPwzPS0nj762cj41_bZOrP87GUoROZ2x_iZ8GIQy5m2S3pAHKuC8Rb0YX7KW1nRnNvv6qZo6CoI6GZQudEL8OyPIUeu70juo-W_F5Jst6HIHPjbYkZzX3_gJNmy5C52kYcf3wCa6lnQmI4TOL4hGybiptSqJLnMyrhakliteEHz0OtwXgZ2Rc3K7EnYmNWvg5yW20rSVL_kM95cXd8MRba5RoCYaxBUNRcZMVjCluck4tgg6BDeFFIWQOnQQJteYVeRC6TyWJkT3KGXyvAhjYbkM92GrnJX2CxAlHFOKiKpQ2KhCWUcoq6DArIfJgPXgpDVjOq_VMlLMMpzpU2_6NGCpM30PDlsjp82iWaRBhHCGoXOx--eqG8PdcRi6tLOlGxNKhCiIW3twUPtk9abWmT2Qa95aDXBS2us9GGFeUruJqK__PfMHbI_ukuv0enxz9Q26gcvK_YnFQ9iqnpf2CKFLlX33gfoXde3r5A
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3fT9swED4BkypeEBsbKz-Gkaa9mTg_aru8oW5VCwQhjUp9ixzb0ZjWUNEg_n3OTlJa9saTpdhWortz_J2-82eA70IZJwAQ0T7ThiZaCJprpmmYhEmEc5j1l02kN3w0SS6nvenKVV--aF_n92flv9lZef_H11bOZzpo68SC23QgeOJ0xoK5KYJN-NCLMcjaRL0hEGQUhi3yxRgTtbymO7cZqL_VzNEQ1EmhbEMnxj80Ah25vjP9BzffVk2ubEPDXdhp8CO5qL_zI2zY8hN00oYh3wObqlrWmYwQPj8jIiXjpt6qJKo0ZFwtSC1ZvCD46HW4LwQ7Jxfk91LcmdTMgZ-X2krRVsLkM0yGv-4GI9pcpUB10utXNOY503nBpAp1HmKLwIOHuhC84ELFDsYYhZmF4VKZvtAxukhKbUwR97kNRfwFtsqH0n4FIrljSxFVFRIbWUjrSGUZFZj5MBGxLvxozZjNa8WMDDMNZ_rMmz6LWOZM34Wj1shZs3AWWZQgpGHoYOw-XXZjyDseQ5X24cmNiQXCFMSuXdivfbJ8U-vMLog1by0HODnt9R6MMi-r3UTVwbtnnkDn9ucwux7fXB3CduQSc39o8Qi2qscne4zopcq_-Th9AebA7Pc
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Maternal+Hookworm+Infection+and+Its+Effects+on+Maternal+Health%3A+A+Systematic+Review+and+Meta-Analysis&rft.jtitle=The+American+journal+of+tropical+medicine+and+hygiene&rft.au=Ness%2C+Tara+E&rft.au=Agrawal%2C+Vedika&rft.au=Bedard%2C+Kathryn&rft.au=Ouellette%2C+Lara&rft.date=2020-11-01&rft.pub=Institute+of+Tropical+Medicine&rft.issn=0002-9637&rft.eissn=1476-1645&rft.volume=103&rft.issue=5&rft.spage=1958&rft_id=info:doi/10.4269%2Fajtmh.20-0503&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0002-9637&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0002-9637&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0002-9637&client=summon