Effect
of
breast-feeding
patterns
onhuman
birth
intervals
P. W.
Howie
and A.
S.
McNeilly
M.R.C. Unit
of
Reproductive
Biology,
University
of Edinburgh,
CentreJor Reproductive
Biology,
37 ChalmersStreet,Edinburgh
EH39EW,
U.K.An
adequate
inter-birth interval is ofgreatimportance
because it enablesamothertorecoverherphysical
and emotionalstrength
betweenpregnancies
andconfersuponthe childadvantages
of betterhealth anddevelopment (Morley,
1977).
Breastfeeding
is thenaturally
evolved method ofensuring
anadequate
inter-birth interval but thecontraceptive
effect of breastfeeding
has beenlargely
dismissed indeveloped
countriesonthegrounds
that it is anunreliablemethod offamily
planning
for individual mothers(Kamal
etal.,
1969).
The use of artificialcontraception
varies verywidely
in differentcountries,
being
muchhigher
indeveloped
nations than in the poorerdeveloping
countries(Text-fig. 1).
Wheretheuseofartificialcontraceptives
islow,
breastfeeding
is themost
widely
used method of birthspacing
andassumesmajor demographic importance.
It isimportant,
therefore,
that the factorscontrolling
lactationalinfertility
should be understood sothat
guidelines
canbedeveloped
whichwillallow motherstomaximize thebirth-spacing
effect of breastfeeding
to their ownadvantage.
Indeveloped
countries,
few mothers choose torely
onbreast
feeding
forfamily planning although
anincreasing minority
mayfind breastfeeding
tobean attractive method of
spacing
theirfamilies,
thereby avoiding
thepotentially
adverse side-effects ofcurrently
availablecontraceptive
methods. Abetterunderstanding
ofhow breastfeeding
mediates itsbirth-spacing
effect may lead to thedevelopment
of newcontraceptive
methods which will try to imitate this
naturally
evolved method offertility
control(McNeilly,
1979).
Developed countries Middle Income countries Poor countries USA UK JAPAN POLAND MEXICO PERU DOMINICAN REPUBLIC JORDAN INDIA PAKISTAN GHANA ZAMBIA =1 =1 ) 20 40 60 %Contraceptiveusers 80 100Text-fig.
1.Contraceptive
usageby
married women aged 15-44 years in differentcountriesbyeconomicstatus.Source:
Population
Reference Bureau Inc.Washington
D.C.,U.S.A.*
Reprintrequeststo:Dr A.S.McNeilly.
t
Present address:Departmentof Obstetrics &Gynaecology,NinewellsHospitaland MedicalSchool,UniversityofDundee,Dundee,U.K.
0022-4251/82/040545-13S02.00/0
This paper will describe the methods which have been used to
investigate
lactationalinfertility
and discusshowdifferentbreast-feeding
patternsinfluencehumanbirth intervals.Methodsof
assessing
lactationalinfertility
Lactational
infertility
can be measured in three different ways:(1) by
the duration of theinterbirth
interval,
(2) by
the duration of lactational amenorrhoea and(3) by
the return of ovulation. These methods presentdifferentproblems
ofinterpretation
andacomplete picture
oflactational
infertility
canonly
be achievedby
considering
all the information which has beengathered
from these differentsources.Interbirth interval. The ultimate test of
fertility
is pregnancy and severalreports
have demonstrated that breastfeeding
increases the interval betweenpregnancies
(for
summary, see vanGinneken,
1977).
Forexample,
twostudiescompared
the timeto nextconception
innursing
and
non-nursing
mothers from Alaskan Eskimo(Berman,
Hanson &Hellman,
1972)
and rural Indianpopulations (Potter,
New,
Wyon
&Gordon,
1965). Despite
the wide differences in climate andculture,
theconception
rates were similar in the twopopulations
andconception
occurred sooner in thenon-lactating
thanlactating
mothers(Text-fig.
2). Considering
the timeuntil 50% of the mothers conceived
again,
breast-feeding
conferred an additionalfertility
protection
of 14 months in the Indian women and 10months in the Eskimo women;assuming
that these intervals
repeated
themselves between successivepregnancies,
this would meanthatnon-nursing
women would have almost double the number of children than the breastfeeding
women overthesametimeperiod.
^ Non-lactating --Lactating O Eskimo •RuralIndian 6 12 18
Months post partum
24
Text-fig.
2. Cumulative conception rates since last pregnancy inlactating
and non-lactatingmothers. Data forEskimos fromBermanetal
(1972),
Indianruralfrom Potteretal.(1965).Rosa
(1975)
hasattempted
toquantify
thecontraceptive
effect of breastfeeding
indeveloping
countries and hascompared
its contribution tofertility
protection
with that ofartificial
contraceptives.
Assuming
additionalfertility protection
of 8 months in rural mothers and of4 monthsin urbanmothers,
Rosa(1975)
estimatedthat,
in thecourse of 1 year, breastfeeding
contributed over 31 IO6couple
yearsofcontraceptive
protection; by comparison,
theknown sales of artificial
contraceptives
contributed 24 IO6couple
years offertility protection
overthesametimeperiod.
Knodel(1977)
haspointed
outthat thedemographic
consequencesofbreast
feeding
arecomplex
because thecontraceptive
effects of breastfeeding
onpopulation
growth
arereduced,
at least to some extent,by
the lowermortality
rates among breast fedbabies. There can be no
doubt, however,
that breastfeeding
hasprofound implications
inDespite
the clear evidence that breastfeeding
is associated withprolonged
interbirthintervals,
itcannotbe assumed that breastfeeding
perseisdirectly
responsible
for this effect. In manycultures,
particularly
inAfrica,
sexual taboos areimposed
onnursing
mothers andreduced
frequency
ofintercourse couldexplain,
at leastin part, thefertility-inhibiting
effect of breastfeeding. Contraceptive
practices during
lactation could also influence the interbirth interval and the use of coitusinterruptus,
forexample,
cannot be monitored on the basis ofcontraceptive marketing figures.
Anexample
of how behavioural factors can influence theinterbirth interval was demonstrated
by
Chen, Ahmed,
Gesche &Mosley (1974)
during
theirdetailed
prospective
study
inBangladesh.
They
found thattheconception
rates after thereturnofpost-partum menses werelowerinfishermens' wives than in farmers'
wives,
probably
becausethefishermenwereabsent from home for
longer periods.
Itisessential, therefore,
toknow what behavioural variablesmight
influence the interbirth interval before theepidemiological
evidence ofmoreprolonged
birthspacing
canbedirectly
attributedtobreastfeeding
itself.Lactational amenorrhoea. Thereturn of menstruationpost partum has been used in many
studies as an indirect index of resumed ovulation
(see
vanGinneken,
1977).
This method isconvenient because it is easy tomeasure andcanbe
applied
tolarge populations. Many
studies have shown thattheduration ofpost-partumamenorrhoea islonger
innursing
thannon-nursing
mothers(for
summary, seeBuchanan,
1975).
Innon-nursing
mothers,
the duration of post-partum amenorrhoeaaverages about 3months,
but amongnursing
mothers it maylast formore than 2 years. It is also clear that
fertility
ismarkedly
reducedduring
theperiod
oflactational amenorrhoea. Chen et al
(1974)
calculatedthat,
during
18 months oflactational amenorrhoea inBangladesh,
the pregnancy rate was less than 5 per 100 women years ofexposure which
compared
well with many artificialcontraceptive
methods. The duration of lactational amenorrhoea is muchlonger
in rural than in urban communities(van Ginneken,
1977)
because rural mothers breast feedmoreintensively
andforalonger
time.Much valuable information hasbeen
gathered
from thestudy
oflactational amenorrhoea but itsvalidity
depends
upon theassumption
that thecapacity
of breastfeeding
to prevent pregnancy is limited to the duration of lactational amenorrhoea. It is well known that breastfeeding
does not postpone pregnancyindefinitely
and 2-10% ofmothers conceiveduring
theperiod
of lactational amenorrhoea(Badraoui
&Hefnawi,
1979).
There is also evidence(see
below)
that thefecundity
of breastfeeding
womendoes not return tonormal after the returnofmensespost partum. It
is, therefore,
desirable to have information from studies whichdirectly
measurethe
resumption
of ovulationduring
thepost-partumperiod.
Detection
of
ovulation. Most studies which haveattempted
todefine thetiming
ofovulation after childbirth have used endometrialbiopsy (Lass,
Smelser &Kurzrok, 1938;
Topkins,
1943;
Udesky,
1950;
El-Minawi &Foda,
1971),
basalbody
temperature
(Sharman, 1951; Cronin,
1968),
cervicalmucus orvaginal
cytology (Perez,
Vela,
Masnick&Potter,
1972)
as markers ofovulation but these methods present
problems
ofinterpretation. During
lactation,
thehistology
of theendometrium mayshowinadequate
co-ordination ofmaturationsigns
characteristic of the normal menstrualcycle, making
it difficult to determine whether ovulation has occurred(El-Minawi
&Foda,
1972).
Ideally,
endometrialbiopsies
should be taken in thepre-menstrual
phase
and,
in the absence ofregular
menstrualcycles,
the correcttiming
ofbiopsies
can bedifficult to achieve.
Biopsies
taken on the firstday
ofbleeding,
ashappened
in severalstudies,
maybe unreliable markers of ovulation.Temperature
chartsduring
lactationmay showamuch shorterplateau
in thepre-menstrual phase (Cronin, 1968) making
precise interpretation
difficult.As an alternative to these
methods,
the use ofplasma
orurinary
steroid concentrationsprovides
objective
evidence ofovulation and enables aquantitative
estimate ofmenstrualcycle
adequacy.
Rolland,
Lequin,
Schellekens & deJong
(1975)
usedplasma
steroid levels to show that ovulation returned morequickly
in mothers who discontinued breastfeeding early
in thepuerperium
but the studies were not continuedbeyond
100days
post partum.Urinary
total oestrogen andpregnanediol
excretion can be used to monitor ovarian follicularactivity
andovulation
(McNeilly,
Howie &Houston,
1980)
and thisnon-invasive method has enabled us tomonitor 10
bottle-feeding
and 27breast-feeding
mothersfromdelivery
untilfirstovulation.1000r
500 -—
>
4 6 8 10 12 14 16 Weeksafterdelivery
Text-fig.3. Return of ovarian
activity (urinary
total oestrogens >10pg/24
h)
and ovulation(urinary pregnanediol
>1mg/24
h)intheearly puerperium
inabottlefeeding
mother..E o CD o 2^ ( TJ E 150 100 50 Solidfood 6000 r8 „ 6
J-g
™ 2 wg-S 4 6 8 1012141618202224262830323436384042444648505254Weeks afterdelivery
Text-fig.
4.Delayed
return ofpost-partum ovarianactivity
and ovulation in abreast-feeding
The
inhibitory
effects of breastfeeding
are illustratedby
the pattern of endocrine eventsleading
totheresumption
of ovulationinatypical
bottlefeeding
(Text-fig. 3)
andatypical
breastfeeding (Text-fig.
4)
mother. Inthebottle-feeding
mother,
basalprolactin
levels had returned tothe non-pregnant range within 4 weeks post partum and this was followed
by
anearly
resumption
of ovarian follicularactivity
(total
urinary
oestrogens > 10µg/24
h)
andmenstrua¬tion. Ovulation
(urinary
pregnanediol
> 1mg/24
h)
did not occurduring
the firstcycle
butresumed in the second and third
cycles.
In thebreast-feeding
mother,
basalprolactin
levels fellprogressively
assuckling
duration was reduced but remained above the non-pregnant range until the cessation of breastfeeding
at 40 weeks post partum. Ovarianactivity
and ovulation weresuppressed
until 44 weeks post partum when the firstanovulatory cycle
was followedby
menstruation at 47 weeks. After the first post-partumcycle,
there was aninterval of 7 weeks before the next menstruation which was followed
by
a normalovulatory
cycle.
Considering
the time of first ovulation in the total group of 10bottle-feeding
and 27breast-feeding
mothers,
the bottle feeders ovulated between 6 and 15 weeks post partumcompared
with 15-68 weeksinthe breast feeders. Thisfinding
is consistent withprevious
reports
(Udesky,
1950; Sharman, 1951; Cronin, 1968;
Perez etal,
1972)
and indicates that amajor
part of the
antifertility
effect of breastfeeding
can be attributed to the inhibition of ovarianfollicular
development
andovulation.Components
of theinterbirth intervalThe interbirth interval consists of three
phases,
thephase
of lactationalamenorrhoea,
themenstruating
interval(which
is the interval between thereturn ofpost-partum menstruation andnext
conception)
and thelength
ofgestation
itself.Only
theperiod
ofgestation
isrelatively fixed,
the durations of lactational amenorrhoea andthemenstruating
intervalvarying widely
betweenpopulations
and between individuals within thesepopulations.
Itis,
therefore,
important
toconsider the
timing
andfrequency
of ovulationsduring
lactational amenorrhoea andduring
themenstruating
interval.Ovulation
during
lactational amenorrhoea. Aspreviously
discussed,
fertility
issubstantially
reducedduring
thephase
of lactational amenorrhoea butbetween2 and 10% ofnursing
mothers conceive before first post-partum menstruation. This is animportant practical point
because it means that the return of menstruation cannot be used as an indication of when to resumecontraception.
Using
endometrialbiopsy
as a marker ofovulation,
Udesky (1950) reported
thatovulationduring
lactationwasfollowed eitherby
menses orby
pregnancy.Thisfinding
has beensupported
by
our own studies(Howie,
McNeilly,
Houston,
Cook &Boyle, 1981)
and indicates that recurrentovulationsdonottakeplace
throughout
thephase
of lactational amenorrhoea. There issome
dispute
about thefrequency
of ovulation in thecycle
before the end of lactationalamenorrhoea,
the estimatesvarying
from 14%(Udesky,
1950),
23%(Cronin, 1968)
and 33%(Howie
etal,
1981)
to 75%(Perez
etal,
1972).
The different estimates of ovulationfrequency
during
lactational amenorrhoeamay bepartly explained by
the differentmethodsusedtoassessovulation but are more
likely
to be due to the differentsuckling
patterns ofthepopulations
studied. It has been shown that the
longer
that the firstmenses isdelayed during
lactation,
the morelikely
isthefirstcycle
tobeovulatory (Perez
etal, 1972;
Howieetal,
1981).
Theimpact
of differentsuckling
patternsuponpost-partumovulation is discussed below.Ovulation
during
themenstruating
interval. There is less informationaboutthefrequency
of ovulation in breastfeeding
mothers who have resumed menstruation and it has beensuggested
that thecapacity
ofprolonged
breastfeeding
toprevent
pregnancy is limited totheperiod
ofduring
themenstruating
interval. Chenetal(1974)
studied theconception
rates afterthereturnof
post-partum
mensesinnursing
mothers and found thatthey
weremuch lower than would beexpected
in anon-nursing
group ofwomen(Tietze,
1968)
who were notusing contraception
(Text-fig.
5).
Similarly,
Potter etal,
1965)
found pregnancy rates of 22 and 32% innursing
mothers at 3 and 6 months after first mensescompared
withcorresponding figures
of 39 and47% in mothers who
experienced
a neonatal death.During
themenstruating
interval,
thefrequency
ofanovulatory cycles
increased,
being
estimated at55%(Lass
etal,
1938)
and 42%(Howie
etal,
1981).
Reducedfecundity
amongstnursing
mothers is furthersupported by
the increased intervals between menstrualperiods, compared
withcycles
innon-nursing
mothers(Sharman,
1951;
Berman etal,
1972;
Howie etal,
1981),
which suggests a disturbance ofnormal
rhythms during
lactation.12 6
Months
Text-fig.
5.Conception
rates in (#) nursing mothers after the return ofpost-partum menses(Chen
etal, 1974)and in(o) non-nursing
womenusingnocontraception (Tietze, 1968).
Using plasma
steroid concentrations as a marker ofovulation,
Duchen &McNeilly (1980)
foundalowerincidenceof
ovulatory cycles during
lactation than would beexpected
in anormalpopulation.
Anexample
of an individual mother who hadrecurrentanovulatory cycles
during
lactation is shown in
Text-fig.
6. After the introduction of solidfood,
basalprolactin
levelsOÍ c >. coro ;~ TJ -· -* c-cn -o E 100r 50 Solid food
IMllríTfr-
»I · 1 )<*&§
3000r 2 4 6 8 1012141618202224262830323436384042444648505254Weeks afterdelivery
returned tothe pregnant range and there were 5
anovulatory cycles (urinary pregnanediol
<1mg/24
h)
before ovulation resumed aftercomplete weaning.
We have studied the levels ofurinary
steroid excretion in 54cycles during
lactation andcompared
them with the levels in 30cycles
after lactation and 27cycles
innon-pregnant controls(Text-fig.
7).
During
lactation,
themean
(±s.e.m.)
level ofurinary pregnanediol
in the lutealphase
were 0·93 ± 0-09mg/24
hwhich was
significantly
lower than the mean level of 1-62 ± 0-15mg/24
h incycles
afterlactation and 2· 13 ± 0-83
mg/24
h in thenon-pregnantcontrols.These resultssuggested
ahigh
incidence of
cycles
which were either anovular or characterizedby inadequate
lutealphases.
Levels of total
urinary
oestrogenexcretion(calculated
asthemeanof the4levelsthroughout
thecycle)
were 10-3 ± 1-0µg/24
h incycles
during lactation,
12-2 ± 1-3µg/24
h incycles
afterlactation and 14-1 ± 1-7
µg/24
h incycles
fromnon-pregnantcontrols. Thiswasconsistent withthe
hypothesis
that the defective luteal functionmight
have itsorigins
in abnormal folliculardevelopment (McNeilly
etal,
1980).
3-1 Menses œ.(b)
4 -3 -2 -1 O
Weeksbeforemenses
(C)
Text-fig. 7. Excretion of
urinary
total oestrogen andpregnanediol
in menstrualcycles
(a)during
lactation(n
=54), (b)
after lactation(n
=30)
and(c)
innon-pregnantcontrols(n =27).
Valuesare mean±s.e.m.
The combined evidencesuggeststhat the
menstruating
intervalisassociated withareductionof
fecundity
which,
however,
is lesscomplete
than it isduring
thephase
of lactational amenorrhoea.Effect of
suckling
uponfertility
It is
important
to understand the effect which differentsuckling
patterns have upon the restoration offertility
so thatappropriate
advice canbegiven
tonursing
mothers who wishtoprolong
the interbirth interval for aslong
aspossible.
It is well known that thephase
oflactational amenorrhoea is much shorter
during
partial
ascompared
with full(unsupplemented)
breast
feeding (Sharman,
1951;
McKeown &Gibson,
1954;
Perez etal,
1972;
Chen etal,
1974).
Gioiosa(1955) reported
that,
out of 500 birth intervals in mothers who breastfed,
46(9-2%)
conceivedduring
lactation but 40 of these(87%)
conceived when theweaning
process wastaking
place.
Gioiosa(1955)
concluded that thefertility protection
associated with breastfeeding
lasted for9 monthsormore,provided
thatno additionalsupplementary
orcomplemen¬
taryformulawasused.
It is
clear,
therefore,
thatsuckling
is amajor
variable in the control ofpost-partumovulationbut
relatively
few studies haveattempted
tomeasurethesuckling
stimulus. Konner & Worthman(1980)
havereported
that theprolonged
interbirth intervals ofupto4 years amongthe nomadic!Kung
huntergatherers
are associated with veryfrequent suckling
bouts,
which last foronly
2min every 15 min. This suggeststhat very
frequent suckling
exerts aprofound inhibitory
effect uponreproduction.
In
Rwanda,
ruralwomenbreast feed ondemand and 50% conceiveagain
within 23 monthsafter
delivery;
by
contrast, in urban women, breastfeeding
isoperated
on a morerigid
schedulewith fewer
feeding episodes
and 50% of mothers have conceivedagain
within 9 monthspost partum(Bonte, Akingeneye,
Gashakamba,
Nbarutso &Nolens,
1974).
In a series ofcross-sectional
studies,
Delvoye,
Badawi,
Demaeged
&Robyn (1978)
found thatprolactin
levels were related both tothe duration oflactational amenorrhoea and tothefrequency
ofsuckling.
By
extrapolation,
these data suggest that the duration of lactational amenorrhoea is related tothe pattern of
suckling
frequency.
These various studiespoint
to theprofound
effect whichdifferent
suckling
patternsexertuponpost-partumfertility.
Infantfeeding
patternsand thetimeoffirst
ovulation.Fromour ownprospective
studies,
theinfant
feeding
patterns werecompared
between mothers who ovulated before 30 weekspostpartum,those who ovulated between 30 and 40 weeks postpartumandthose who ovulated after 40 weekspost partum. The mothers who
postponed
ovulation forlongest (>40 weeks)
had alonger
total duration of breastfeeding
than did those in the other two groups, but there wereotherdifferences between thegroupsas illustrated in
Text-fig.
8;
the mothers who ovulated after40 weeks maintained
suckling
duration andfrequency
at thehighest
levels,
introducedsupplementary
food mostslowly
and maintainednight
feeds forlongest.
The maintenance ofnight
feeds(defined
as asuckling episode
betweenmidnight
and 08:00h)
may beimportant
because a
long
interval withoutsuckling
could allow thehypothalamic-pituitary-ovarian
axissufficient timetorecover andresumeovulation. This
study suggested strongly
that therewas aninverse
relationship
between the use ofsupplementary
foods and thestrength
ofthesuckling
stimulus,
and that theearly
andabrupt
introduction ofsupplements
might play
animportant
partin relationtothe
resumption
ofpost-partumovarianactivity
and ovulation. •>40 weeksO30-40 weeks
<30 weeks
Weekspost partum
Text-fig.
8.Comparison
of infantfeeding
in mothersovulating
before 30 weeks(N
=7),
between 30 and 40(N=9)andafter40 weeks(N=9)postpartum.Valuesare mean+s.e.m.
Effect of supplementary food
onsuckling
and ovulation. The criticalimportance
ofsupplementary
food wasemphasized
by
centring
the levels ofsuckling frequency
andsuckling
duration round the time at which
supplements
wereintroduced(Text-fig.
9). Suckling
durationand
suckling frequency
for the whole cohort ofbreast-feeding
mothers remainedrelatively
constant until
supplements
weregiven,
after which bothfellabruptly.
Thesechanges
insuckling
werereflected in thebasalprolactin
concentrationsand,
beforetheintroductionofsupplements,
no mother had ovulatedalthough
four had evidence of ovarian folliculardevelopment.
Aftersupplements, progressively
more mothers had evidence of ovarian folliculardevelopment
and52% had ovulated within 16 weeksof
introducing
supplementary
food.Text-fig.
9. Meansuckling
duration,suckling
frequency,
basalprolactin
andovarianactivity
inwomen
(N
=27)
before and after the introduction ofsupplementary
food. Values are mean±s.e.m.Broken line indicates upper limitfornon-pregnantwomen.(FromHowieetal,1981.)
In
Text-fig.
10,
thefeeding
patternsin the 52% who ovulated within 16 weeks ofintroducing
supplements
arecompared
with the 48% who continued to suppress ovulation over that time.The mothers who ovulated reduced
suckling
morerapidly
and weaned moreabruptly.
Thestronger
suckling
stimulus amongst those who continued tosuppress ovulationwasreflected inhigher
meanbasalprolactin
levels which remained above thenon-pregnantrange.Sequence
ofeventsleading
topost-partumovulationFrom the data
presented
in this paper, it ispossible
to formulate ahypothesis
of the eventsleading
to the return of post-partum ovulation. Inbottle-feeding
mothers,
plasma prolactin
concentrationsreturntonormal within a few weeks of
delivery
and there isanearly resumption
of ovarian
activity
and ovulation. Inbreast-feeding
mothers,
prolactin
values are elevated andovarian function is
suppressed,
theextentofthatsuppression
being dependent
uponthestrength
and duration ofsuckling;
thesuckling
stimulus is underminedby
theuse ofsupplementary
foodwhich
indirectly
encouragestheresumption
ofovarianactivity.
Intheir detailedstudy,
Perez et100 -Supplementary food I +12 +16 10 +14
Text-fig.10.
Comparison
ofinfantfeeding
patterns and basalprolactin
between(o)
mothersovulating
within 16 weeks(N
=14)
and( )
motherssuppressing
ovulation ( =13)
afterintroduction of
supplementary
food. Values are mean +s.e.m. The broken line indicates theupperlimit fornon-pregnantwomen.* <0-01. (FromHowieetal, 1981.)
Table 1.Percentage of
breast-feeding
mothersgivingsupplements
(occasionalorregular)
ineconomically
advantaged, urban poor and rural groups of different countries (from W.H.O. Collaborative Study on
Breast
Feeding, 1979)
Country Group
2-3 months
6-7
months Country Group
2-3 months All 46-8 96 Chile All 30-7 100 Advantaged Poor Rural 60 59 59 Advantaged Poor Rural 67-8 49-2 49-3 Guatemala 38-6 85-3 Advantaged Poor Rural 93 51 13 Advantaged Poor Rural 86-1 63-5 35-0 100 91 86 Philippines Advantaged Poor Rural 84 36 41 Advantaged Poor Rural 38-3 36-0 49-0 84 95 76 India Advantaged Poor Rural 52 5 1
ovulation or pregnancy but
they
did not define thesuckling frequency
which constituted full breastfeeding
in theirpopulation.
Nevertheless,
it is clear that theearly
andregular
use ofsupplementary
food will have a detrimental effect onthecontraceptive
effect of breastfeeding
and itmustbea matterofconcernthat theW.H.O.Collaborative
Study
onbreastfeeding
foundsuch a
high
use ofsupplementary
foods among mothers fromdeveloping
countries within 2—3monthspostpartum
(Table 1).
Otherfactors
influencing
lactationalinfertility
It has been
suggested
that malnutrition may have animpact
on the duration of lactationalamenorrhoea,
independent
of breastfeeding
itself(Thomson, Hytten
&Black,
1975). Bongaarts
(1980)
has reviewed the evidence and concluded that chronic malnutrition had arelatively
minor effect on
fertility;
forexample,
themedian durations of amenorrhoeainlow,
medium andhigh
nutritiongroupsfromBangladesh
were21-2,
20-4 and 20-2 monthsrespectively (Huffman,
Chowdhury, Chakbarty
&Mosley, 1978).
Extreme fooddeprivation
during
famine, however,
exertsa
large
buttemporaryreduction infertility
(Bongaarts, 1980).
Lunn, Prentice,
Austin & Whitehead(1980) compared
two groups ofbreast-feeding
Gambian
mothers,
onereceiving
a caloriesupplement,
the otherreceiving
no suchsupplement.
The mothers
receiving
the caloriesupplement
had lowerprolactin
concentrations and menstruatedmorequickly.
This evidencesuggested
that maternal nutritionmight
have aneffect onfertility
butinterpretation
of data is made difficultby
thetendency
ofpoorly
nourishedmothers to breast feed for
longer
and suckle morefrequently
than well nourished mothers(Prema,
Naidu &Kumari,
1979).
Future studieswhichinvestigate
the effects of nutritionuponthe
contraceptive
effectsofbreastfeeding
should haveobjective
measures both ofsuckling
andnutritionalstatus.
Age
has also beenimplicated
as a factor ofimportance,
because the duration of lactationalamenorrhoea tendstobe
longer
in older than inyoungerwomen(Jain,
Hsu,
Freedman&Chang,
1970).
Practical
implications
oflactationalinfertility
Reliability
of
breastfeeding
as acontraceptive
method. It has to berecognized
that breastfeeding
cannot be relied upon as a guaranteeagainst
pregnancy for individual mothers. Theplace
of breastfeeding
infertility
control has to be considered in the context of all the other factors which arepertinent
to aparticular population
andto each ofthe individuals within thatpopulation.
Theimportance
ofbreastfeeding
as amethod of birthspacing
willdepend
upontheavailability
of alternativecontraceptive
methods,
thewillingness
of the mothers to use themethods and the averageduration ofuseof any
particular
method.These factors varywidely
indifferent communities and breast
feeding
should beregarded
as a method offertility
controlwhich should be
exploited
along
with,
rather than insteadof,
alternative methods ofcontraception.
Nevertheless,
breastfeeding
continues tohaveanimportant
rolein birthspacing
throughout
theworld,
andenthusiasticbreast-feeding,
characterizedby frequent
andenergetic suckling,
canexert a
high degree
offertility protection, particularly
during
thephase
of lactationalamenorrhoea.
Birth
spacing
indeveloping
countries. The mainimportance
of breastfeeding
as acontraceptive
method is indeveloping
countries where alternative methods offamily
planning
are usedinfrequently.
It is clear that the modern methods of infantfeeding,
withtheearly
andfrequent
useofsupplements,
willhaveprofound
implications
onfertility
andpopulation
growth.
from the burdens of
childbearing,
this must be matchedby
increasedavailability
and use ofalternative
contraceptive
methods. The abandonment ofprolonged
breastfeeding,
without alternativecontraception,
will shorten interbirth intervals andgreatly
increase the burdens onindividual mothers and
community
resources.Breast-feeding practices
haveimplications
for infantgrowth,
neonatal infection and birthspacing.
Infantfeeding
policies
should bedesigned only
afterrecognizing
theimportance
of all thesecompeting
factors.Strategies of
contraception.
Potter,
Masnick & Gendell(1973)
havepointed
outthat,
inmany
communities,
acontraceptive
method may be usedonly
for a finiteperiod
of time. If acontraceptive
method isbegun immediately
afterparturition,
there will beanoverlap
between thetime when the
contraceptive
is used and theperiod
ofpost-partum
anovulation whenprotection
isnotneeded.By
delaying
theintroduction of thecontraceptive
method,
theextentof theoverlap
is
reduced,
and thepotential contraceptive efficiency
increased. Forexample,
inBangladesh,
Potter et al
(1973)
calculated that if the use of artificialcontraception
weredelayed
until 6monthspost partum,
only
1 in200womenwould have conceivedby
that time. Morestudies arerequired
in different communitiestodevelop strategies
whichexploit
post-partuminfertility
andcontraception
tothebestadvantage.
Birth
spacing
indeveloped
countries. Indeveloped
countries themajority
ofbreast-feeding
mothers will use acontraceptive
method. Some of thesemothers, however,
dislike theinconvenience and the
potential
side-effects of the various methods andregard
thepossibility
ofusing
thebirth-spacing
effect of breastfeeding
as an attractive alternative. These mothers willhaveto breast feed
enthusiastically
and acceptthat the method is notabsolutely
reliable. Morework is
required
todefinetheminimumsuckling frequency
and duration whicharenecessarytoinhibit ovulation
reliably
but a number ofguidelines
canbetentatively suggested
tothose who wish to maximize thecontraceptive
effect. Mothers should feed on demand and usesupplementary
bottles asinfrequently
aspossible.
When it becomesnutritionally
necessary for solid foodtobegiven
tothebaby,
this should beintroducedgradually
andnotabruptly.
Mothers should beencouraged
tobreastfeedatnight
and avoidlong
intervals betweensuckling.
These
guidelines lay
theemphasis
onsuckling
andrequire
much enthusiasm on the part ofthe mother. Breast
feeding
is acomplex
physiological
process with functionsbeyond
those of infant nutrition alone. It isimportant
that,
inthefuture,
the advice and supportwhichis offeredtomothers should be formulated with full realization of all the
implications
which breastfeeding
has for both maternal and child health.References
Badraoui, M.H.H. & Hefnawi, F. (1979) Ovarian functionduringlactation. In Human Ovulation, pp.
233-241. Ed.E.S.E.Hafez.Elsevier/NorthHolland BiomedicaiPress,Amsterdam.
Berman, M.L., Hanson, K. & Hellman, I.L. (1972)
Effect of breastfeedingonpostpartummenstruation,
ovulation and pregnancy in Alaskan Eskimos. Am. J. Obstet.Gynec.114,524-534.
Bongaarts,J.(1980)Does malnutrition affectfecundity?
A summary of evidence. Science, N.Y. 208,
564-569.
Bonte,M.,Akingeneye,E.,Gashakamba,M.,Nbarutso,
E. & Nolens, M. (1974) Influence of the socio-economic level on the conception rate during
lactation.Int.J. Fértil.19,97-102.
Buchanan, R. (1975) Breast-feeding—aid to infant health and fertility control. Population Reports,
SeriesJ,No.4,49-67.
Chen, L.C., Ahmed, S., Gesche, M. & Mosley, W.H.
(1974) A prospective study of birth interval
dynamics in rural Bangladesh. Pop. Stud. 28,
277-297.
Cronin, TJ. (1968) Influence of lactation upon
ovulation. Lancetii,422—424.
Delvoye, P., Badawi, P., Demaeged, M. & Robyn,M.
(1978) Long lasting lactation in association with
hyperprolactinaemia and amenorrhoea. In Progress inProlactinPhysiologyandPathology,pp. 213-232. Eds C.Robyn&M.Harter.Elsevier/NorthHolland BiomedicaiPress,Amsterdam.
Duchen, M. & McNeilly, A.S. (1980) Hyperprolactin¬ aemia and long-termlactational amenorrhoea. Clin. Endocr.12,621-627.
El-Minawi, M.F. & Foda, M.S. (1971) Post-partum lactation amenorrhea. Am. J. Obstet. Gynec. Ill,
Gioiosa, R. (1955) Incidence of pregnancy during lactation in 500 cases. Am. J. Obstet. Gynec. 70,
162-174.
Howie, P.W., McNeilly,A.S.,Houston,MJ., Cook,A. &Boyle,H.(1981)Fertilityafter childbirth: effect of breast feeding on ovulation and menstruation. Br. med. J.283,757-759.
Huffman, S.L., Chowdhury, A.M.K., Chakbarty, J. &
Mosley, W.H. (1978) Post-partum amenorrhoea: how is it affected by maternal nutritional status?
Science,N.Y.200,1155-1157.
Jain, A.H., Hsu, T.C., Freedman, R. & Chang, M.C.
(1970) Demographic aspects of lactation andpost¬ partumamenorrhoea.Demography7,255-271. Kamal,I., Hefnawi, F., Ghoneim, M.,Talaat,M., Younis,
N., Tagui, A. & Abdalla, M. (1969) Clinical bio¬ chemical and experimental studies on lactation. I.
LactationpatterninEgyptianwomen.Am.J. Obstet.
Gynec.105,314-323.
Knodel,J.(1977)Breastfeedingandpopulation growth.
Science,N.Y.198, 1111-1115.
Konner,M.&Worthman,C.(1980) Nursing frequency,
gonadal function and birth spacing among !Kung
huntergatherers.Science,N.Y.207,788-791.
Lass, P.M., Smelser,J. & Kurzrok, R. (1938) Studies
relating to time of human ovulation, iii. During
lactation.Endocrinology23,39-43.
Lunn, P.G., Prentice, A.G., Austin, S. & Whitehead,
R.G. (1980) Influence of maternal diet on plasma
prolactinlevelsduringlactation. Lanceti,623-625.
McKeown. T. & Gibson, J. A. (1954) A note on
menstruation and conception during lactation. J. Obstet.Gynaec.Br.Emp. 61,824-826.
McNeilly,A.S.(1979)Effects of lactationonfertility.Br.
med. Bull.35, 151-154.
McNeilly, A.S., Howie, P.W. & Houston, MJ. (1980) Relationship of feeding patterns, prolactin and
resumption of ovulation post-partum. In Research
Frontiers in Fertility Regulation, pp. 102-116. Eds
G. I.Zatuchni,M. H. Labbok & J. J. Sciarra.Harper
&Row,New York.
Morley,D.(1977) Biosocialadvantagesofanadequate
birth interval. J. biosoc.Sci.,Suppl.4,69-81.
Perez, ., Vela,P.,Masnick,G.S. &Potter,R.G.(1972)
First ovulation after childbirth: the effect of breast
feeding.Am.J.Obstet.Gynec. 114,1041-1047.
Potter, R.G., New, MX., Wyon, J.B. & Gordon,J.E.
(1965) Applications of field studiesto research on
physiologyof humanreproduction.Lactation and its effects upon birth intervals in elevenPunjab villages,
India. J. Chron. Dis. 18,1125-1140.
Potter, R.G., Masnick, G.S. & Gendell, M. (1973)
Postamenorrhoeic versus post-partum strategies of
contraception. Demography 10,99-112.
Prema, K., Naidu, A.N. & Kumari, S.N. (1979) Lactation and fertility. Am. J. clin. Nutr. 32,
1298-1303.
Rolland, R., Lequin,R.M.,Schellekens,L.A.&deJong,
F.A.(1975)The role ofprolactinin the restoration of ovarian functionduringtheearlypost-partumperiod in the human female. I. Study during physiological
lactation. Clin. Endocr.4, 15-25.
Rosa, F.W. (1975)The role of breastfeeding infamily
planning. WHO ProteinAdvisory GroupBull.5,No.
3,5-10.
Sharman, A. (1951) Menstruation after childbirth. J.
Obstet.Gynaec.Br.Emp. 58,440-445.
Thomson, ., Hytten, F.E. & Black, A.E. (1975) Lactation and reproduction. Bull. Wld Hlth Org. 52,337-349.
Tietze, C. (1968) Fertility after discontinuation of intrauterine and oralcontraception.Int. J. Fértil. 13,
385-389.
Topkins, P. (1943) The histologie appearance of the endometrium during lactation amenorrhea and its
relationship to ovarian function. Am. J. Obstet.
Gynec.45,48-58.
Udesky,I.C. (1950)Ovulation inlactating women.Am.
J. Obstet.Gynec.59,843-848.
van Ginneken, J.K. (1977) The chance of conception