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https://doi.org/10.1093/tropej/fmab097
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2 Effect of Breastfeeding on Pregnancy
ABSTRACT
Background: Breastfeeding is beneficial to both mother and infant. However, overlap of lacta-
tion with pregnancy and short recuperative intervals may impact mothers nutritionally. We
aimed to investigate the possible effects of pregnancy during breastfeeding.
Methods: In October 2018, we searched systematically in nine electronic databases to investigate
any association of breastfeeding during pregnancy with fetal and/or maternal outcomes. The study
protocol was registered in PROSPERO (CRD41017056490). A meta-analysis was done to detect
Research articles with the following criteria were studies were considered as heterogeneity, we used a
excluded: in vitro studies, animal studies (rats, random-effects model following the method of Der
mouse, dogs), overlapped data, cannot extract data, Simonian and Laird. Otherwise, we used a fixed-
abstract, case-report, case series, thesis, book chap- effect model following the Mantel–Haenszel method
ters, abstract/poster for a conference paper and [20]. We used the Q statistic and I2 test, which
articles have no full texts (authors’ responses, editori- describes the percentage of variability in the effect
als, comments and letters), reviews and meta-ana- estimates that is because of heterogeneity beyond
lysis. Three reviewers separately performed titles and sampling error to evaluate the heterogeneity between
Quantitative synthesis
1 Shaaban/2015/ • All successive multiparous November 2013 to Egypt 540 • The prevalence of mis- Interview using Prospective-cohort Women who did not
Egypt [32] women who were pregnant December 2014 carriage, maternal structured study give lactation to
introduced to the enrollment anemia, hemorrhage, questionnaire their last child
Maternal and Child Health elevated blood sugar, and lived in areas
Centers in the first trimester of elevated blood pressure, away from recruit-
pregnancy (under 12 weeks placental separation and ments center
pregnant) and be followed until eclampsia between the were excluded.
labor. two groups.
• Qualified subjects were divided • Time, method of deliv-
into two groups based on the ery and onset of compli-
point of time they got pregnant: cations during delivery.
during breastfeeding or after • Fetal status at birth,
weaning. weight at birth and need
for referral to a neonatal
care unit.
2 Merchant/1990/ • According to the weaning time 1969 to 1977 Guatemala 504 • Maternal supplement Interview Longitudinal data 48% of the women
Guatemala [37] of the previous child and the intake, body store Observation from a nutrition- provided data on
concept of indexing the child, • Fetal growth Intervention supplementation more than one
pregnancies are divided into two (Supplement trial pregnancy to the
groups: (1) non-overlap if wean- provider) study sample.
ing 2 weeks after conception
and (2) overlap if weaning >
2 weeks after conception.
• Study sample: When there is an
overlap, 55.7% only breastfed
during the first trimester of
pregnancy, 41.1% continued
breastfeeding to the second tri-
mester and 3.2% continued to
the third trimester.
3 Madarshahian/ • The overlap group consisted of April to December Iran 320 • Pregnancy problems, • Interview using Comparative Study
2012/Iran [13] women who breastfeed their 2008 nutritional change, ges- questionnaire
older children three to five times tational age, birth weight • Observation
per day during their current • Pattern and duration of
pregnancy, for at least 30 days. breastfeeding
(continued)
4 Albadran/2013/ • Study population: Pregnant September 2011 to Iraq 215 cases Proportion of miscarriage, Prospective Case–control study
Iraq [33] women who breastfed during September 2012 280 controls preterm, full term and
pregnancy. Case group: preg- birth weighs
nant women who breastfed over
24 weeks of pregnancy. Control
group: pregnant women who
breastfed during 24 weeks of
pregnancy.
• Exclusion: women less than 18
and over 35; with diseases such
as diabetes mellitus, thyroid dis-
eases, sickle cell anemia; with
history of recurrent miscarriage
and preterm births; multiple
pregnancies.
5 Ishii/2009/ • Cases: The pregnancy was con- 1996 to 2000 Japan 110 cases • Proportion of term and Retrospective review Retrospective All children were
Japan [34] firmed before 8 weeks of gesta- 774 controls preterm births, the outcome of matched control continued to
tion, and women who were miscarriage each pregnancy study breastfeed even
breastfeeding at the time of • Frequency of lactation from patient after a
diagnosis were recruited. In • Gestational age at records miscarriage.
these cases, 38.7% continued weaning
breastfeeding to 12 weeks,
27.4% to 28 weeks, 33.6% con-
tinued after 28 weeks and 7.9%
continued breastfeeding infants
even after delivery.
(continued)
6 Pareja/2015/ Continue breastfeeding until at least March 2006 to April Peru 95 cases Compared the proportion of Interviewing using Case–control study
Peru [12] the 28th week of pregnancy. 2007 150 controls women who breastfed structured
> 28 weeks of pregnancy, questionnaire
between two groups: Reviewing and
SGA and non-SGA extracting informa-
tion from clinical
chart
7 Marquis/2002/ Continue breastfeeding during the July 1998 to January Peru 133 Compare birth events, new- Prospective Prospective-cohort Families of included
Peru [10]f third trimester of pregnancy. 2000 born characteristics and study pregnant women
growth outcomes at had some indica-
1 month between group tors of a better
overlap and non-overlap economic status
compared to
those were
excluded.
8 Marquis/2003/ Continue breastfeeding during the July 1998 to January Peru 133 Evaluating the link between Prospective Prospective-cohort
Peru [38]f third trimester of pregnancy. 2000 an overlap with macronu- study
trients and immunologic-
al agents in milk,
newborn urinary IgA,
morbidity of mother and
infants.
9 Merchant/1990/ Breastfeeding> 2 weeks after 1969 to 1977 Guatemala 102 • Maternal supplement Prospective Data from random-
Guatemala [11] conception. consumption and fat ized control trial
storage
• Birth weight
(continued)
10 Ayrim/2014/ All pregnant women who continued June 2004 to Turkey 165 Compared between two Retrospective Cross-sectional Intrauterine growth
Turkey [29] breastfeeding during the preg- December 2011 groups in body mass reviewed the clin- study retardation was
nancy period. index before pregnancy, ical records not observed in
weight gain during preg- two groups.
nancy, birth weight,
Apgar score, obstetric
adverse events (anemia,
miscarriage, intrauterine
growth retardation,
preterm delivery).
11 Sengul/2013/ Women who experienced preg- June 2006 to June Turkey 61 Compared between two Observation Case–control study None in the breast-
Turkey [28] nancy while breastfeeding. 2009 groups in terms of pre- feeding group
pregnancy body mass continued to
index, gestational weight breastfeed after
gain, birth weight, obstet- 20 gestational
ric complications (missed weeks.
abortion, intrauterine
growth restriction, pre-
term labor).
Qualitative synthesis
12 Hassanabadi/2013/ • Overlap: Women who breastfed July 2009 to April Iran 320 Birth weight, height, head Observation Case–control study
Iran [35] their older children during 2010 circumference and preg-
current pregnancy. nancy outcome between
• Non-overlap: Women who two groups
weaned their older children at
least 3 months before
pregnancy.
13 Shaaban/2008/ Conceived the present pregnancy June 2006 to June Egypt 2617 • Prevalence of women Using an interview- Cross-sectional 29 women (4.4%)
Egypt [6] during breastfeeding. 2007 who got pregnancy er-administered study conceived in the
during lactating period structured first 6 months
• Pregnancy intention questionnaire postpartum, 100
• Breastfeeding pattern women (15.1%)
conceived before
menstruation
resumed.
(continued)
14 Bohler/1996/ Breastfeeding concurrent with April to September East Bhutan 113 • Average growth rate Semi-structured Cross-sectional
Himalayas [42] pregnancy. 1990 during weaning interview study
• Relation between con-
ceived while lactating
and early cessation of
lactation
15 Merchant/1991 • Short overlap subgroup: women 1969 to 1977 Guatemalan 504 The effects of breastfeeding Prospective Data from random-
Guatemala/[46] weaned their baby in the first during pregnancy on the ized control trial
trimester. nutrition implication of
• Long overlap subgroup: women mothers, infants and
weaned their baby in the second fetuses.
or third trimester.
16 Ismail/2009/Egypt Breast milk samples from 45 lactat- Not mention Egypt • 45 case and Total chemical composition Prospective Case–control study
[44] ing pregnant women, whose dur- • 45 control of milk, protein compos-
ation of pregnancy range from ition and immune
8–11, 12–15, 16–19 and 20– components.
40 weeks. Only nine women,
who were at 8–11 weeks, can be
followed up to the third
trimester.
17 Moscone/1993/UK Overlap criteria was not specified. September 1985 to La Leche League 57 Change in flow/frequency Questionnaire by Retrospective
[45] Jun 1986 of breast milk email
18 Pike/1999/Kenya Overlap criteria was not specified. August 1993 to July Ngisonyoka, 68 Questionnaire Cross-sectional
[30] 1994 Turkana interviewed study,
prospective
19 Siega-Riz/1993/ Women who were lactating during 1983 to 1987 Cebu Longitudinal 1367 Patterns of weight gain Comparative study
Philippines [31] pregnancy. Health and during pregnancy
Nutrition Survey
20 Molitoris/2019/USA Women who were lactating during 2002 to 2015 National Survey of 10 661 Risk of miscarriage Extract data from Cross-sectional
[36] pregnancy. Family Growth several waves of study,
the National retrospective
Survey of Family
Growth
Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N
e
1 Ismail/2009/ (18–36) – 45 a (combined) 45 -
Egypt [44]
2 Shaaban/2008/ 28.09 5.84 2617 a (combined) 2.83 c 1.7 2617 a
Egypt [6] 0.79 d 1.2 2617 a
3 Shaaban/2015/ 28.8 6.18 270 30.5 5.2 270 2.39 d 1.54 270 2.64 1.18 270
Egypt [32]
4 Merchant/ 30.2 6.8 249 28.7 6.7 252 5.4 d 2.8 253 5.8 3 247
1990/
Guatemala [37]
5 Madarshahian/ 28.4 4.6 80 29.6 5.7 240 2.9 d 1.3 80 2.8 1 240
2012/Iran [13]
6 Albadran/ 27.6 0.28 215 27.9 0.27 280 3.3 1.6 215 3.5 1.7 280
2013/Iraq [33] 2.2 1.6 215 2.5 1.7 280
7 Ishii/2009/ 28.7 3.4 110 29.1 2.9 774 -
Japan [34]
8 Pareja/2015/ 27.3 6.01 227 a (combined) 2.26 c 1.51 228 a 10.71 5.27 128 Note: There are
Peru [12] 1.93 d 1.3 228 a two subgroups:
SGA and
non-SGA.
Combined
mean and
SD of both
subgroups ¼
10.27 6 5.27
(n ¼ 128)
9 Marquis/2002/ 25.9 5.5 68 25.9 4.7 65 2.1 d 1.3 68 2.1 1.1 65 1 mo postnatally 26.2 3.8 68 25.9 3.6 65
Peru [10] f
10 Marquis/ 35 – 44 a (combined) 29 – 1 mo postpartum 26.2 0.5 68 25.9 0.4 65
2003/Peru [38] f
11 Bohler/1995/ 26.8 – 98 a (combined) –
Himalayas [41]
12 Bohler/1996/ 29.6 – 40 26.8 – 40 4.0 – 40 2.8 – 40
Himalayas [42]
13 Ayrim/2014/ 24.3 4.9 45 23.2 3.3 120 - Not mentioned, even no 25.4 4.4 45 26.4 3.7 120 7 3.4 45 13 5.6 120
Turkey [29] word ‘BMI’
are found
(continued)
Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N
14 Sengul/2013/ 25.3 4.9 39 23.2 3.3 22 2.5 c 0.9 39 2.3 0.7 22 Not mentioned, even no 26.4 4.4 39 25.7 3.7 22 10.6 3.6 39 11.8 3 22
Turkey [28] 1.4 d 0.9 39 1.3 0.6 22 word ‘BMI’
are found
15 Pike/1999/ 28.09 5.63 68 a (combined) Pre-pregnancy Monthly changes in Tri 1 2.20 20 0.56 20
Kenya [30] and third maternal weight Tri 2 0.21 22 1.11 22
trimester gain (kg) for Tri 3 0.32 34 0.42 34
each gestational
trimester
16 Siega-Riz/ (Not state clear) Monthly total Tri 1 and 2 0.88
1993/ Pre-pregnancy, first þ weight gain Tri 3 1.24
Philippines [31] second þ third between
trimester women who
were lactating
during pregnancy
17 Moscone/ 29 4.14 57 a (combined)
1993/UK [45]
the mean gravidity for all mothers was 2.32 pregnan- them were of ‘high’ risk of bias as well as two ‘mod-
cies with an average parity of 2.83 and 2.91 babies erate’ risk and one ‘low’ risk of bias.
for lactating and non-lactating groups, respectively.
In the same context, the mean calf circumference of Maternal outcomes and complications
133 infants was 33 cm in lactating mothers and 32.6 during pregnancy
cm in non-lactating mothers. Regarding to maternal Pooling three studies [32–34] of 1919 mothers
body mass index (BMI), mean of BMI in lactating showed no significant difference between lactating
was 26.04 kg/m2 and 26.16 kg/m2 in non-lactating and non-lactating ones of spontaneous abortion [OR
Fig. 3. Meta-analysis of full-term healthy (A), preterm delivery (B) and preterm labor (C) between lactating and non-
lactating pregnant.
16 Effect of Breastfeeding on Pregnancy
pregnancy and breastfeeding on colostrum compos- Meta-analysis result of two studies showed signifi-
ition and morbidities’ rate among both mother and cant higher prevalence of intrauterine growth restric-
offspring. In the second day postpartum, lactose and tion (IUGR) in women who got pregnant during
lysozyme components were higher and lactoferrin lactation compared with those occurred after wean-
component was lower in breastfeeding group (BFG) ing [OR (95% CI) ¼ 3.59 (1.91–6.71), p ¼ 0.000]
compared to non-breastfeeding group (NBFG), re- [32]. In another study, Ishii [34] reported one case
spectively. One month postpartum, BFG showed a of artificial induced preterm labor due to IUGR. On
decreased IgA concentration as compared to NBFG. the other hand, a case–control study found no evi-
Moreover, infants of BFG were a five-time more sus- dence of the association between breastfeeding dur-
ceptible to develop a cough, for at least 7 days, com- ing late pregnancy and elevated risk of SGA [12].
pared to NBFG (Supplementary Table S5). These studies identified IUGR or SGA using the
Effect of Breastfeeding on Pregnancy 17
same criterion ‘fetal birth weight less than 10th per- In addition, a recommendation from the American
centile after adjusting for gestational age’. Academy of Pediatrics mentioned that breastfeeding
should continue for at least 12 months, and subse-
DISCUSSION quently for as long as mutually desired [4].
Breastfeeding is considered as the most effective inter- Moreover, our analysis did not find any significant
vention of ensuring child survival and health. relationship between concurrent pregnancy in
Exclusive breastfeeding until 6 months and continuing women and the risk of adverse maternal outcomes
up to 2 years are recommended by both WHO and and delivery complications.
children, Moscone and Moore [45] found that the wants and the adequate nutritional regime for these
majority of weaning from breastfeeding initiated by woman should be aware of.
the infant took place during the second trimester.
The middle 3 months of pregnancy corresponds to a SUPPLEMENTARY DATA
period of diminution in volume of breastmilk which Supplementary data are available at Journal of Tropical
reported by 70% of pregnant women. However, the Pediatrics online.
infants born were healthy and appropriate for gesta-
tional age. Despite pregnancy during breastfeeding is ACKNOWLEDGMENT
We would like to thank the reviewer for the detailed com-
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study to examine the association between breastfeeding analyses be undertaken and interpreted? Stat Med 2002;
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