Breast Feeding Fertility and Family Plan PDF

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 25

See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/244944601

Breastfeeding, Fertility, and Family Planning

Article in The Global Library of Women s Medicine · January 2009


DOI: 10.3843/GLOWM.10397

CITATIONS READS

4 47

1 author:

Miriam Labbok
Gillings School of Global Public Health, University of North Carolina at Chapel Hill
166 PUBLICATIONS 3,128 CITATIONS

SEE PROFILE

All content following this page was uploaded by Miriam Labbok on 02 May 2014.

The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.
Breastfeeding, Fertility, and Family Planning

Miriam H. Labbok, MD, MPH


Professor of the Practice of Public Health, and Director, Carolina Breastfeeding
Institute, formerly, the Center for Infant and Young Child Feeding and Care,
Department of Maternal and Child Health, School of Public Health, University of
North Carolina, Chapel Hill, North Carolina, USA

INTRODUCTION
RESEARCH DESIGN ISSUES IN THE STUDY OF BREASTFEEDING AND
FERTILITY
PHYSIOLOGY OF LACTATIONAL INFERTILITY
BREASTFEEDING AND FAMILY PLANNING
REFERENCES

INTRODUCTION
Breastfeeding is associated with many maternal and child health benefits,1, 2, 3 including a
delay in fertility return postpartum. This has been recognized for centuries; medical
literature from Aristotle to the Renaissance, and, occasionally, thereafter, noted that
women who suckle are less likely to become pregnant. This physiological response was
forgotten or disbelieved in scientific circles of the mid 20th century as the use of
commercial infant formula displaced breastfeeding in industrialized settings, and family
planning methods became more widely available. However, recent scientific evidence,
compiled both by social and biomedical sciences, demonstrating the population level
impact of breastfeeding on fertility and the biologic basis of lactational infertility, has
reinitiated interest in breastfeeding and the mechanisms related to lactational infertility. If
we allow breastfeeding to deteriorate further, the increase in fertility in settings with
limited family planning use would be significant, and very difficult to remedy.4, 5
Today, breastfeeding is being rediscovered and has become the normative initial infant
feeding behavior; however, the optimal patterns of breastfeeding that are also associated
with fertility reduction are not as yet the norm in many industrialized settings. Optimal
breastfeeding for child health is defined by the World Health Organization (WHO) as six
months exclusive breastfeeding6 followed by continued breastfeeding with age-
appropriate complementary feeding for up to two years or longer.7 The Healthy People
2010 goals for the United States include at least 75% initiation, with 50% continuation to
six months and 25% to one year, and exclusive breastfeeding among 40% for three
months and 17% for six months. Data from the US Centers for Disease Control and
Prevention8 and National Center for Health Statistics now reflect achievement of the
initiation goal. Although rates fall off over time, this still means that a majority of
postpartum women will be introducing some form of contraception during breastfeeding.
However, there remains rapid fall off in continuation and exclusivity (see Table 1).
Therefore, for optimal maternal and child health outcomes, physicians must increasingly
have the knowledge and skills to support both optimal breastfeeding and appropriate
family planning introduction during lactation.
Table 1: Breastfeeding in the United States and globally9

Initiation 6 months 12 months Exclusive 3 Exclusive 6


months months

US 74.2 ± 1.2 43.1 ± 1.3 21.4 ± 1.1 31.5 ± 1.3* 11.9 ± 0.9*

Developing > 95 - 40 ^ - 38**


settings

World > 90 - 39 ^ - 38 **

* percent exclusive for the full duration; **percent exclusive in a sample of 0-6
months; ^ at 20-23 months of age
Good clinical practice will depend on achieving knowledge and skills to address issues
associated with breastfeeding and fertility, including basic anatomy and physiology as
they apply to both lactation and the fertility aspects of breastfeeding, and the proper
counseling and timing of the provision of contraceptives. The practitioner may also need
the knowledge and skills to support conception during breastfeeding, when warranted.

RESEARCH DESIGN ISSUES IN THE STUDY OF BREASTFEEDING AND


FERTILITY
There are research design and analysis issues that have increased the publication of
apparently conflicting findings in published studies on breastfeeding and fertility.
Definitions of Characteristics under Study
The term breastfeeding is used to describe a wide variety of behaviors and physiologic
states in both mothers and the children. A commonly used definition in the 1960s and
1970s was that of the commercial infant formula industry, which defined breastfeeding in
relation to a formula norm. Breastfeeding was generally defined by a ‘yes’ or ‘no’
response, with limited consideration of pattern or exclusivity. Industry interests are to sell
product, so the term exclusive breastfeeding was used when breastfeeding with no
formula use. However, this definition allowed for other food and drink to be given, and
still be defined as ‘exclusive’ breastfeeding. In the past, the US Women, Infants and
Children program (WIC) defined a mother-infant pair as breastfeeding if they ever
breastfed at all; others have used definitions that describe varying time periods. These
definitions, which reveal little about infant nutrition or about maternal physiology,
continue to be used by some researchers, creating apparently conflicting findings for the
casual reader of the literature.
Many journals now accept definitions that may be more reflective of the maternal and
infant behavior and its potential impact on their physiology.10 This definitional schema:
• defines the feeding pattern during a single period in time, perhaps a 24-hour
recall
• defines only breastfeeding and records, but does not define, other forms of
feeding
• demands attention to both the maternal and the child's involvement
• differentiates breastfeeding from human milk feeding.
• encourages additional description of the behavior beyond the basic terms in
Table 2
The schema also suggests that researchers and program planners note frequency,
timing and length of intervals, age of the child, use of expressed milk, how other
milks are given, whether pacifier use allowed, and, where applicable, the type, timing,
and amount of other feeds. If used, such a schema would allow differentiating
between the specific behaviors and the physiologic consequences. Only by including
these issues can one assess the patterns which impact on physiology in addition to
nutritional outcomes, very important in light of the differential in the physiologic
responses to different modes of milk expression and direct suckling.11
A widely used set of definitions was developed subsequently by the WHO, modified
from that presented above, but simplified such that they are appropriate to describe
infant nutritional intake, but are less relevant for the understanding of maternal and
child physiology.12 This newer set of definitions does not take into account the impact
on maternal physiology and potential milk maintenance, the potential differences in
behaviors within the definitions used, nor the differences between direct breastfeeding
and indirect human milk feeding, in terms of immunologic and other factors. These
two sets of definitions are compared in Table 2.
Table 2. Physiology-based and infant nutrition-based definitions of breastfeeding

Term Physiologically based Infant intake based definition of


definitional schema* World Health Organization

Breastfeeding The child directly ingests The child has received breastmilk
breastmilk from the mother's (direct from the breast or
breast. expressed).

Breastmilk Milk is expressed and given to Not defined.


feeding the infant.

Exclusive Feeding is exclusively from the The infant has received only
breastfeeding breast. No other liquid or solid breastmilk from his/her mother or
from any other source enters a wet nurse, or expressed
the infant's mouth. breastmilk, and no other liquids or
solids with the exception of drops
or syrups consisting of vitamins,
mineral supplements, or
medicines.

Almost exclusive Allows occasional other tastes Not defined.


of liquids, traditional foods,
Term Physiologically based Infant intake based definition of
definitional schema* World Health Organization
vitamins, medicines, etc.

Predominant Not defined. The infant's predominant source of


nourishment has been breastmilk.
However, the infant may also have
received water and water-based
drinks (e.g. sweetened and
flavored water, teas, infusions);
fruit juice; oral rehydration salts
solution; drop and syrup forms of
vitamins, minerals and medicines;
and ritual fluids (in limited
quantities). With the exception of
fruit juice and sugar-water, no
food-based fluid is allowed under
this definition.

Full Includes exclusive and almost Includes exclusive breastfeeding


breastfeeding exclusive, as already defined. and predominant breastfeeding, as
defined above.

Full breastmilk Receives expressed breastmilk, Not defined.


feeding in addition to breastfeeding.

Partial Mixed feeding designated at Not defined.


high, medium or low. Methods
for classification suggested
include percentage of calories
from breastfeeding, percentage
of feeds that are breastfeeds,
among others. Any feeding of
expressed breastmilk falls
under this category.

Complementary Other food or milk given in The child has received both
feeding addition to breastmilk, thus breastmilk and solid (or semisolid)
displacing breastmilk intake. food.

Token Minimal, occasional Not defined.


breastfeeds (for comfort or with
less than 10% of the nutrition
provided thereby).

*Calls for age of child; feeding frequency and intervals; use of bottle, cup, spoon,
pacifier; and feeding of expressed milk be recorded for each definition where
available.
The immense variability in lactation and breastfeeding behaviors necessitates large
samples sizes to fully explore the impact of the differences. However, the relatively
short durations of lactation, and the prevalence and use of contraceptives that mask or
interfere with physiologic changes have limited the number of such studies completed
in industrialized countries. Therefore, much of what we understand is derived from
small clinical studies, some of which have not been able to control for even the most
important variables, such as sucking stimulus or age of infant. Other studies have used
quasi-experimental or epidemiological methods, with intervention and assessment at
the population level rather than the individual level.

Sampling Frame and Sample Size


Immense differences in lactational behaviors indicate that large samples would be
necessary to control for this variable alone. However, the relatively short durations of
lactation, and the prevalence and use of contraceptives that mask or interfere with
physiologic changes, limit study in industrialized countries. Therefore, much of what
we understand is derived from limited clinical studies, some of which have little
control over sucking stimulus or age of infant or that information is inferred from
larger prospective studies with limited neuroendocrinologic elements.
Selection Bias in Selection of Cases and Controls
Breastfeeding patterns are skewed, with more breastfeeding occurring among those
earlier postpartum. With or without breastfeeding, normal maternal physiology
undergoes changes postpartum. Therefore, the choice of infant age group/time
postpartum studied can significantly influence physiologic outcomes. This is further
complicated by the difficulty in random assignment of these breastfeeding and
complementary feeding behaviors. It is not ethically possible, nor probable that
groups of women would agree, to be assigned to breastfeed or not breastfeed. It is
even more unlikely that infants will cooperate with the timing of their hunger or the
intensity of their suck at any particular time. This may lead to confounding, associated
with the factors that may influence self-selection into one pattern of feeding or
another.
Recall Bias
Many studies include data from mothers whose children have long since stopped
breastfeeding. Their recall may be biased by subsequent child health events or by the
breastfeeding experience of subsequent pregnancies. CDC recently explored recall
and found many definitional flaws and inconsistencies.
Analytic Plan and Techniques Used
Proper selection of statistical approach is vital. There are many textbooks designed for
the clinician or occasional researcher. The analysis plan should be designed before
data are gathered, because it may dictate to some extent the sample frame and size.
However, it remains important to reassess the plan after data are collected. The data
set may have insufficient numbers in proposed subgroups due to limited variability
within the sample, or may not reflect other assumptions used in planning. For
example, if all women in the sample breastfeed for about the same length of time,
there will be insufficient variability in the data set to assess the biologic impacts of
varying durations of breastfeeding.
Selective Presentation of Findings due to Journal Space Limits
Because journals frequently limit the length of articles, important facts in the
interpretation of the findings may be inadvertently omitted. Also, negative results are
rarely accepted for publication.
Misinterpretation or Confused Conclusions, and Conviction-Based Bias in
Presentation
In statistics, terms such as association or determinant may be misinterpreted as
meaning causation. Two things may be statistically significantly associated but have
no biologically meaningful relationship. Although we like to think that scientists are
unbiased, each works from personal understanding of the issue in question. This may
affect how the hypothesis is stated and tested, and which data are presented. If
findings do not support the author's hypothesis or do not achieve statistical
significance, it is often difficult to find the energy—or the journal willing—to publish
it. Finally, discussion and conclusion sections of papers may include statements that
overstate or reinterpret what the findings show.
These difficulties compound the problems of data collection and analysis in this already
complex area of study.

PHYSIOLOGY OF LACTATIONAL INFERTILITY


The anatomy of the breast and the hypothalamic-pituitary axis for release of prolactin and
the production of breast milk may be found elsewhere in this text. These same structures
are integral to the mammary-hypothalamic-pituitary-ovarian axis that mediates lactational
infertility. The current understanding of the physiology of this feedback system is derived
from studies of the different systems under conditions of lactation and nonlactation.
Because of the difficulties in studying these phenomena, as previously outlined, this
section summarizes current understanding and presents also a summary of studies that
confirm the underlying conclusions presented here.
Summary
Suckling at the breast, especially with active stimulation of the nipple and areola and the
structures that underlie them, stimulates an inhibition of the pulsatile release of
gonadotropin-releasing hormone (GnRH) from the hypothalamus, which in turn,
disorganizes the pulsatility and levels of follicle-stimulating hormone (FSH) and
luteinizing hormone (LH). The result of the disruption of the levels of LH, and the
sometimes reduced levels of FSH, is suppression of the development and release of a
viable follicle and ovum. Over time, as erratic pulsatility begins, there will be some
ovarian follicular development with increases in inhibin B and estradiol. When this
occurs, there can be a paradoxical re-suppression of fertility, rather than the stimulation of
ovulation seen in non-breastfeeding women13 (see Fig. 1). With increasingly normal
pulsatility, associated with decreases in the suckling stimulus, a resumption of apparently
normal follicle growth occurs associated with a normal increase in estradiol. However,
this is often associated with the formation of an inadequate corpus luteum. Eventually,
there is a return to normal ovulatory menstrual cycles.14
Oxytocin release from the posterior pituitary, which stimulates the let-down reflex,
allowing milk to flow through the capillary-like mammary tubules, has not as yet been
linked to suppression of fertility; however, its establishment is necessary for successful
lactation, and, as such, is a necessary part of the lactational infertility.15 Plasma prolactin
levels that are associated with milk production in the early days postpartum are less
associated with milk production as time progresses,16 and these levels would seem to have
a limited role in the feedback system that suppresses ovulation. In addition, maternal
nutritional status is much less important than the pattern of infant breastfeeding; however,
the maternal nutritional status may impact the feeding pattern. While much of the
underlying physiology remains to be elucidated, the basic parameters of this feedback
system may be seen in Fig. 1.

Fig. 1. Mammary-hypothalamic-pituitary-ovarian feedback system: suppression of


fertility and menses related to breastfeeding.
Discussion of Research
A recent symposium attempted to bring together scientists to discuss the current
understanding and gaps in the knowledge concerning the physiologic basis of
lactational infertility. Based on exploration of published and unpublished literature,
three stages were identified:17 early postpartum lactational amenorrhea, continued
lactational amenorrhea, and menses return.
The early postpartum period, in this context, is the 6–8 weeks postpartum during
which the inhibitory mechanisms of pregnancy continue to produce an impact, with
diminished pituitary response to the hypothalamic release of GnRH. This is possibly
due to reduced activity of the GnRH pulse generator; however, in the first month
postpartum, there is no LH response to a GnRH bolus. Studies of LH activity during
this same period have yielded variable findings, indicating that there may be
individual or behavior-based variation. Another study shows that the LH pulse
frequency is not significantly different from that found in the early follicular phase;
the peak levels, however, are significantly reduced.18 By the second postpartum
month, LH response to a GnRH bolus may be seen, indicating a shift in the
underlying mechanisms.19 This would imply decreased end-organ receptivity, in this
case the pituitary. Opiates do not seem to mediate this shift in humans as they do in
some nonhuman animal models.20 The timing of this shift may be dictated by intensity
and pattern of feeding or by individual physiologic differences.
Those factors that influence the duration of continuing lactational amenorrhea, in
relation to the duration of lactation, are not fully understood. At the same time,
ongoing diminished GnRH and pituitary responsiveness continue in relationship to the
intensity of the suckling stimulus. However, quantifying this phenomenon is difficult.
Other mechanisms are thought to contribute, creating a complex of sometimes-
conflicting feedback loops. These include enhanced or paradoxical negative feedback
of ovarian secretions on the hypothalamic-pituitary axis; failure of positive feedback
actions, lack of stimulation of the hypothalamus; decreased number or function of
GnRH receptors; altered biologic activity of the hormones of ovulation; and a variable
role of prolactin. It was concluded that there is a possibility of redundancy in these
mechanisms.15
Attempts to elucidate the role of prolactin have found little direct involvement in the
suppression of fertility. One important study included 20 women, with 24-hour blood
sampling every 10 minutes, at either four or eight weeks postpartum, at either time of
introduction of supplements, at first menses while continuing breastfeeding, and in the
follicular phase of the first cycle after weaning. Results included that the pattern of
prolactin levels was responsive to breastfeeding pattern, but that there was no
relationship between the plasma concentrations, day or night, and the duration of
amenorrhea. There was, however, a strong and statistically significant correlation
between the timing of introduction of food or liquids and the duration of
amenorrhea.21, 22 Feeding the infant any foods in addition to breastfeeding prior to six
months of age is associated with about a 4–6 fold increase in the risk of menses return
prior to six months.23 Another study of 10 women in Chile found that women who
returned to fertility earlier exhibited a smaller prolactin response to suckling as early
as the first month postpartum than was found among those with a delayed return of
fertility.24 Although prolactin levels clearly are responsive to suckling, and there is an
association of prolactin response and earlier return of menses, the pattern of prolactin
release is not predictive of fertility return for the individual.
Another long-held hypothesis was that maternal fat stores dictated the duration of
lactational infertility. To investigate the extent to which better maternal nutrition is
associated with a reduction in the duration of lactational amenorrhea, data on 339
mother-infant pairs were analyzed.25 Maternal triceps skinfold was negatively
associated with the length of amenorrhea; once controlled for infant feeding pattern,
the effect was small; only a 0.5-month difference was seen when the 25th and 75th
percentiles were compared. Improved maternal nutritional status by supplementation
was not associated with change in length of amenorrhea if controlled for infant
supplemental feeding. In another study, the effect of body mass index on lactational
amenorrhea became nonsignificant when controlling for lack of formula feeds,
maternal age, and socioeconomic status.26These studies suggest that infant, not
maternal, supplementation influences the duration of lactational amenorrhea, and that
maternal nutritional status has modest influence. In a recent review of the physiology
of lactation, Neville raises the possibility that another hormone associated with
nutritional status, such as the appetite-suppressing hormone leptin, may play a role.27
It may be that the physiology of the negative association of maternal overweight with
breastfeeding initiation and duration28 has an influence on these studies, creating a
bias in which mothers enter the cohort. Although the impact of nutritional status on
lactational amenorrhea is less significant than earlier believed, the factors that mediate
this association remain to be elucidated.
The return of menses during lactation is highly variable, among individuals and
among cultural groupings.29, 30 There are many behavioral and physiologic parameters
that may have some impact on the timing of the return of fertility during lactation.
Clearly, the sucking stimulus is a major variable and accounts for much of the
variation seen. Frequency, with recovery time during the interval between feeds,
intensity of the child's suckling, and hence breast stimulation, and the sensitivity of
the nipple and areola of the breast, may all play a role. There appears to be increased
pituitary responsiveness to GnRH over time; however, the presumed mediation by β-
endorphins or opiates, has not been substantiated in humans. Whether it is dictated by
individual variation in neuroendocrine response to the stimuli, the variation in
bioactivity of specific hormones and end organ, including ovarian, response to the
changes remains to be assessed.
Fertility does not necessarily return immediately with the return of regular vaginal
bleeds. The first cycles during breastfeeding frequently are associated with abnormal
ovulatory activity and luteal phase defects. Studies have found, on average, a gradual
return to normality over the first three cycles. An analysis of survey data found that,
in areas where breastfeeding is practiced physiologically, that is, frequently day and
night with little to no supplementation given, the continuation of breastfeeding after
menses return is associated with significant continuing delay in fertility. In this study,
for each additional month of breastfeeding after menses return, there is about 7.4%
reduction in risk of conception.31 This is thought to be primarily due to ongoing luteal
phase defects.32
Differentiation of the first hormonally induced bleed from continued lochia or
perceived end-of-puerperium bleeding episodes may present an issue for some
women, especially those interested in charting their cycles or predicting the next
bleed. A multicenter multinational study of the return of a hormonally induced bleed,
retrospectively defined as a bleed followed by another bleed within 21–70 days found
that the duration of lochia varied significantly. The conclusion was that among
intensively breastfeeding women, about 11% experienced such a bleed in the first two
months postpartum.33
The suckling at the breast is the major stimulus of the feedback; however, the specific
attributes of the suckling that contribute to the suppression of fertility are not fully
elucidated. Clearly, frequency of the suckling episodes is vital. In the very early
postpartum stage, suckling of 10–12 times a day appears the minimum number necessary
to establish full lactation and fertility suppression. During the second stage, frequency
may be reduced, but increasing intervals between feeds and initiation of or increase in
supplementation are associated with hastened return of both ovulation and return of
menses.31, 34 After menses, or regular bleeds, recurs, frequent suckling continues to be
associated with decreased fertility. Other parameters of the suck stimulus have been
harder to study. In an effort to assess the impact of sucking intensity, a pressure
transducer was attached to the nipple of exclusively breastfeeding women (n = 62) at two
and five months postpartum. Although the efficiency and duration of the suckling, per se,
were not correlated with duration of amenorrhea, the time at the breast in non-suckling
pauses was positively associated with a delay in menses return.35 This may indicate that
sensory stimulation other than suckling alone may have a vital role in the feedback to the
hypothalamus. Possible areas for further exploration include the importance of olfaction
in early mother-infant bonding36 and cosleeping. These areas remain to be studied in
relation to the duration of lactational infertility, and the physiologic impact of behaviors
and sensory stimuli.
BREASTFEEDING AND FAMILY PLANNING
Contraceptive Use During Lactation
Studies of maternal nutritional recovery postpartum and of outcomes of subsequent
pregnancies have shown that spacing of births is necessary for improved outcomes. Child
spacing of about 28 months is suggested as healthiest for pregnancy outcomes in a US-
based population.37, 38 In developing country settings, spacing of this length or longer is
recommended.39 Although breastfeeding alone can result in spacing of this duration, the
individual woman is cautioned not to rely on breastfeeding alone if she wishes to achieve
this goal. Therefore, the introduction and use of family planning during breastfeeding are
important health interventions.
The choice of method should be the woman's, based on complete information on which to
make an informed choice. Counseling is generally necessary to ensure that this fully
informed choice can occur. Generally, contraceptive technology texts emphasize efficacy
as the major criterion for method selection. In fact, women's choices are generally based
on various other factors, including personal experience, a desire to delay or permanently
cease childbearing, lifestyle, and religious influences. She might also be influenced by the
other health impacts of the method on her or her child, in addition to those directly
associated with breastfeeding and contraceptive efficacy. Some of these are presented in
Table 3.
Table 3. Summary of the non-contraceptive health issues associated with the use of
contraceptive methods

Milk quantity and infant growth Passage to infant Maternal health*

Condom – – Reduced HIV and


sexually transmitt
disease infection r

Intrauterine device— Some reports of increase in milk – May be associated


nonsteroidal quantity.40 increased blood lo

Combined oral May decrease milk quantity, even in Infant receives about May lower levels
contraceptives low-dose preparations. 0.1–0.2% of maternal vitamins and mine
dose.41 may have circulat
effects, particular
important immedi
postpartum.

Progestin-only oral Positive effects in studies, anecdotal Infant probably Assumed to be les
contraceptives (POCs) negative effects in clinical practice. receives about 0.1– estrogenic formul
Perhaps dependent on estrogenicity or
Milk quantity and infant growth Passage to infant Maternal health*
related behaviors and stresses. 0.2% of maternal dose.

Depo-Provera (depot Positive. Few studies on use prior to 4– MPA passes at plasma Assumed to be les
medroxyprogesterone 6 weeks postpartum. levels into the estrogenic formul
acetate, DMPA). breastmilk, however
uptake from the
circulatory system is
limited.

Norplant No negative effect. Slightly negative Infant receives about Lowest levels, the
when given before six weeks.42 5–15% of maternal assumed to have l
dose.43 effect.

Vaginal ring with No negative impact on breastfeeding or – Lowest levels, the


progesterone growth.44 assumed to have l
effect.

*Hormonal methods may have long-term health benefits for women including
decreased rates of reproductive tract cancers; methods that reduce menstrual blood
loss would contribute to anemia reduction. (Hatcher R, Rhinehart W, Blackburn R et
al: The Essentials of Contraceptive Technology pp 4–19. Baltimore: Johns Hopkins
School of Public Health, Population Information Program, 1997.)
Table 4 presents the method options categorized by potential impact on breastfeeding,
not on efficacy of the method or the other issues that may be of interest to the
individual patient. (The American College of Obstetrics and Gynecology issued
guidelines on aspects of breastfeeding. The guidelines support this table while
allowing earlier initiation of hormonal methods when appropriate.)
Table 4. Family planning considerations for the breastfeeding woman

Method Failure rates* ‘common’ use/’perfect’ use Breastfeeding and reproductive


health considerations, advantages,
disadvantages

First choice: Nonhormonal methods

LAM 2/0.5 Supports optimal breastfeeding.

Condoms† 15/2 Decreases transmission of HIV and


other infectious diseases that may pas
to the child through breastfeeding.

Diaphragm with 16/6 Size requirement may change


spermicide postpartum and refitting should occur
after 6–8 weeks.

May provide reduce transmission of


Method Failure rates* ‘common’ use/’perfect’ use Breastfeeding and reproductive
health considerations, advantages,
disadvantages
some infections.

Spermicides 29/18 May provide reduce transmission of


some infections.

May provide needed lubrication.

Intrauterine devices 0.8/0.6 Insertion should occur within four day


(IUDs) (nonhormonal, or after four weeks postpartum.
with copper)
(Hormone 0.2/0.2 No effect of IUD or copper on
(progestin) containing breastfeeding.
IUDs)
Reports of reduced perceptions of
discomfort if inserted while mother is
still lactating.

Natural family planning 20/3–5 May require special training for


(periodic abstinence) previous users since signs and
symptoms use in the methods may dif
during lactation.

Some methods may result in prolonge


periods of abstinence during lactation

Vasectomy 0.15/0.1 No impact on any maternal or infant


health parameters.

Tubal ligation 0.5/0.5 May involve a period of separation.

May involve anesthesia, analgesia, bu


rarely necessitates interruption of
lactation.

Second choice: progestin-only methods

Mini-pill 8/0.3 Limited research on use before six


weeks postpartum in lactating women

Injectables 3/0.3 Possible maternal health effects of


progestin use very early postpartum.

Implants 0.05/0.05 World Health Organization recommen


delay for at least six weeks post

Vaginal ring with 8/0.3 World Health Organization recommen


progesterone during
Method Failure rates* ‘common’ use/’perfect’ use Breastfeeding and reproductive
health considerations, advantages,
disadvantages
breastfeeding delay for at least six weeks postpartum

Third choice: methods containing estrogens

Combined oral 3–8/0.3 Estrogenic component may reduce mi


contraceptives/injectables supply, change electrolyte compositio

Combined Injectables 0.3/0.3 World Health Organization recommen


delay for at least six months postpartu
or until exclusive breastfeeding is
ended.

LAM, lactational amenorrhea method.


*Most pregnancy, or failure, rates as presented are from life-table analyses in studies
of women who are not breastfeeding, except as indicated. These rates would be
expected to be lower when used during breastfeeding due the additive impact of to its
fertility suppressive effects. Pregnancy rates presented are based on studies of use
during lactation. (Modified from Hatcher R, Trussell J, Nelson A, et al: Contraceptive
Technology, pp 407-409, 759. Ardent Media, Inc. 2007.45)
Nonhormonal methods are considered the first choice because they have no direct
impact on breastfeeding. The lactational amenorrhea method (LAM), described later
in this chapter, may be used as in introduction to other method selection, or as the
primary method in the early months. In addition to LAM, the choices include
physical, chemical, and temporal barriers, as well as male and female sterilization.
Second choice is the progestin-only methods that have been extensively tested and
found safe in later breastfeeding.46 In the last decade, possible association with
maternal bone loss became an issue. A prospective study of levonorgestrel (Norplant),
progesterone vaginal rings, and CuT380 intrauterine devices (IUDs) found no
difference in bone status among the three groups at months 1 and 12 postpartum, and
at six and 12 months after cessation of lactation.47 There are many studies of vaginal
rings, a method not as yet approved for use in the United States, that show this to be a
safe and efficacious method for lactating women; however, there remain issues of
user satisfaction.
The timing of introduction of progestin-only methods continues to be debated. There
is little in the literature on the use of these methods during the first 4–6 weeks
postpartum among fully breastfeeding women. Assessment of the studies available,
clinical reports, and preliminary guidance from the WHO would encourage caution,
recommending delay of use for at least six weeks postpartum, and calling for further
research concerning this specific situation.
The estrogenic methods, despite their higher efficacy, are considered third choice
because of their known negative effect on milk production. Other concerns, such as
changes in micronutrients, including iron, calcium, copper and phosphorus, seem
unfounded.48, 49 Consideration has been given to whether a woman should switch from
the less efficacious progesterone-only methods to the estrogenic methods at some
point during lactation. An opinion poll of 20 providers considered to be expert in the
field concluded that there is no reason to switch during early lactation but that there is
no problem with doing so after six months postpartum.50
Breastfeeding can significantly reduce menstrual loss and fertility, but cannot alone
provide reliable adequate child spacing for most women. Although further research is
needed to understand all the neuroendocrine mechanisms underlying lactational
infertility fully, clinical studies have outlined the parameters under which
breastfeeding can be reliable. LAM should be considered an option in the complete
picture of informed family planning choice for the lactating woman. This issue is
addressed regularly by the Academy of Breastfeeding Medicine Protocol #13.51
Family Planning Based on the Physiology of Lactation
There has been interest in building on lactational infertility to create a reliable,
efficacious form of family planning for more than 30 years. In the 1970s, researchers
began to publish studies showing that under clinical conditions of full breastfeeding
and amenorrhea, fertility would be a rare event.34 At the same time, Tyson and others
pursued the pituitary-gonadotrophin route, assessing the impact of thyrotropin-
releasing hormone (TRH) and other related hormonal releasing hormones on
fertility.34, 52, 53 More recently, it has been suggested that GnRH agonists might
enhance the impact and duration of lactational infertility.54 These approaches that
enhance or suppress the hormonal feedback system have been associated with
acceptable side effects. Although there is a high correlation of the timing postpartum
of fertility return with previous breastfeeding experience when measured in a
population of women, this is not a reliable indicator for the individual.
Stimulated by these early publications, researchers began to explore the relationship
between breastfeeding patterns, menses return, and fertility suppression to see
whether a noninvasive approach based on an improved understanding of the
physiology might be possible. In 1988, the research findings of several centers around
the world were shared at a meeting at the Rockefeller Bellagio Conference Center,
and the scientists agreed that three criteria (i.e. full breastfeeding, amenorrhea, first
six months postpartum) would be sufficient to serve as a method. These findings
became known as the Bellagio Consensus.55 A few months later, this approach was
presented to a group of family planning service providers at a meeting at Georgetown,
in the District of Columbia, and LAM was developed as a clinical algorithm, and
guidelines were prepared.56
LAM is a postpartum introductory method that includes three criteria for defining the
period of lowest pregnancy risk and then advises immediate commencement of
another method that complements the effects of breastfeeding thereafter. Clinically,
the mother would be asked whether her menses have resumed, whether she is no
longer fully or nearly fully breastfeeding, and whether the infant is six months of age
or older. If the answer to any of these is affirmative, she is advised to begin another
method of family planning, preferably one that will have no negative effects on
lactation (Fig. 2). Counseling includes timely switch to another method compatible
with lactation, and the encouragement of healthy birth spacing of about 2.5–3 years,
allowing for maternal recovery postpartum and postlactation before another
pregnancy commences.
Fig. 2. Lactational amenorrhea method
Because this method is based on behavior, there is no organization in the United
States with the mandate to review its safety. For this reason among others, the WHO,
Family Health International, and the Institute for Reproductive Health (Department of
Obstetrics and Gynecology, Georgetown University) assembled a second
internationally recognized panel. The Rockefeller Foundation approved a second
Bellagio conference that was held to consider the safety and efficacy of the method.
Based on LAM clinical trials and WHO multicenter studies that had confirmed that
fully lactating amenorrheic women have about a 1% chance of pregnancy, this panel
concluded the following:
“The Bellagio Consensus clearly has been confirmed … The efficacy of LAM has
now been well established in prospective studies, and programs should regard LAM
as an additional method that increases the family planning choices for postpartum
women. Lactational Amenorrhea Method should receive the programmatic and policy
support necessary to become available worldwide … Programs should ensure that any
LAM user is able to begin the new method in a manner that ensures continuity of
protection from an unplanned pregnancy."57
This new method of family planning has been found to be highly effective (Table 5).
Table 5. Efficacy of the lactational amenorrhea method

Location Study type Efficacy: life table analysis, %

Chile57 Prospective study with control group. 99.6

Ecuador58 Retrospective-prospective study of LAM 98.8


Location Study type Efficacy: life table analysis, %
acceptors in a family planning clinic.

Philippines59 Prospective clinical study among women 99.0


with previous breastfeeding experience.

Pakistan60 Prospective clinical study among women 99.4


with previous breastfeeding experience.

Rwanda*61 Retrospective-prospective study using 100


client records.

Georgetown/WHO/South-to- Prospective study of LAM acceptors in a 98.5


South multicenter study of variety of settings.
LAM62, 63

WHO multicenter study of Prospective study of lactating amenorrheic 99


lactational amenorrhea64 women.

Multicenter follow-on study*65 Postmarketing study of LAM. 100

LAM use among NFP users66 Prospective study of first menstrual cycle 100
with NFP charting, ultrasound.

Egypt67 Passive LAM use. 98.5

Cochrane Review68 Prospective studies. 98.8–99.1

*Significant loss to follow-up.


This new method is now in use in more than 30 countries, and has been included in
family planning and maternal and child health policy in several countries.69 Duration
of LAM use, which contributes to effectiveness of the method, varied across these
studies, averaging about 4–5 months.70 Duration of the method in common usage has
been shown to depend on ambient breastfeeding norms and maternal commitment, in
addition to physiologic predisposition. LAM may be used no matter what the average
breastfeeding pattern may be, as it is a method for individual use, like all other
methods. Studies have confirmed that there are a significant minority in nearly every
country that could use this method.71
At least one study has shown that LAM provision is associated with a lengthened
birth interval.72 However, on average, while LAM use may well be quite important to
the individual, it will not have a sufficient impact on birth interval alone to allow
women to achieve a healthy interval. Demographic and Health Survey data were used
to explore decisions about timing of contraceptive use among postpartum women. The
findings revealed that policy and program strategies that focus on counseling
immediately postpartum or at a later interval, such as when menses resume, may have
a substantial influence on the use of contraceptives.73 The recommendation to switch
to another method in a timely manner is best accompanied by counseling for at least
3-year intervals between children.
Studies reveal that the major reasons for non-use of this method include lack of health
worker and maternal awareness of the method, belief that there is not sufficient
breastfeeding in their population (despite global and national data that show the
increasing rates of exclusive breastfeeding), fear of some undesirable effect on health,
and concerns about efficacy. Additional reasons for accepting LAM include being
convinced by counseling and intention to use LAM initially before switching to
another method. One study found that occupation outside the home (P=0.01) and
previous knowledge of LAM (P<0.001) emerged as predictors of LAM acceptance.74,
75, 76
These issues are readily addressed with proper information.

LAM has been shown to be efficacious in all settings, even where exclusive
breastfeeding may not be the norm. Even in countries such as the US where exclusive
breastfeeding may only continue for 2–4 months, the method has an important role.
For example, one study found that patterns of exclusive breastfeeding may differ in
different settings, e.g. women in Baltimore breastfed less often but for more minutes
at each feed than did women in Manila. Nonetheless, the mean durations of lactational
amenorrhea were about six months and nine months, respectively, both of adequate
duration for LAM use.
Success in the provision of this method is enhanced when there is adequate
breastfeeding support available to the mother and when she is properly counseled in
those breastfeeding behaviors associated with fertility suppression. Based on the
physiologic responses, LAM counseling should include discussion of optimal
breastfeeding behaviors for both lactation maintenance and fertility suppression, and
the importance of birth spacing and the timely switch to another method of family
planning. Studies indicate that the frequency of the breast stimulation and the
maintenance of short intervals between feeds (no longer than four hours during the
day or six at night) seem to be associated with lactation maintenance.
Advantages and disadvantages of the method include its efficacy and reliability, and
that it expands the ‘contraceptive options’ for women. It has been shown to be an
effective transition method, encouraging initiation of a longer term method in a timely
manner. The method has no additional cost beyond that associated with fully
breastfeeding women and it reduces the need for contraceptive commodities needed to
achieve adequate birth spacing. The disadvantages of LAM include lack of protection
against STIs and that it requires optimal patterns of breastfeeding.58, 77
The term ‘passive LAM use’ is used to describe the situation when the woman has
adhered to the criteria but is not actively aware of the method; when the criteria are in
place, the efficacy is similar to that found among women actively using the method.78,
79
However, to extend the use of the method, support for six months of exclusive
breastfeeding is required, and international guidance recommends six months of
exclusive breastfeeding.80, 81 Work by Dewey and colleagues involved a random
assignment at four months to continue exclusive breastfeeding, or to begin a high-
quality, clean supplement provided free of charge. Two important findings were
noted: there was a significant decrease in the breast milk intake and amenorrhea at six
months was decreased by 20%.82, 83 Further, exclusive breastfeeding women who do
not know about LAM are at risk for not transitioning to another method of
contraception at six months postpartum, while women who were aware of LAM
criteria were likely to transition appropriately.84 Research in the US found
considerable overlap of breastfeeding and contraceptive use; however, many women
did not use contraception.85 A study in Egypt found that women of low empowerment
index in household decisions were more likely to use passive LAM than modern
contraception.86 This may be due to lack of self-efficacy in family planning choices.
Clearly, the use of this method, and the practice of optimal breastfeeding in general,
are linked to lifestyle choices for the mother.
Infertility
In the diagnosis of infertility, breastfeeding and lactational amenorrhea status should
be one of the first aspects of the medical history addressed. Other factors that should
be considered include the possibility of subclinical infection associated with
secondary infertility, and, where appropriate, extreme altitudes.27, 87 This normal
fertility delay may not be welcome among women who wish to plan a subsequent
pregnancy and are not concerned with the public health guidance concerning spacing
of births.
It is not always necessary to advise cessation of breastfeeding in these cases; adjustment
of feeding pattern to favor return of ovulation is a possible alternative. Because hormonal
responses are thought to be greater at night, it is suggested that night feedings be limited,
and that total 24-hour frequency of breast stimulation be reduced. This should not be
recommended unless the infant is independent of the need for breastfeeding for nutrition,
health, and immune system development. Lactational infertility may continue even after
menses appear to be normal, so counseling should include the possibility of an extended
time line, and assurances that optimal maternal nutritional recovery occurs with cessation
of breastfeeding when mother and baby decide, followed by about six months of
nonlactation, nonpregnant status.

REFERENCES

1 Labbok M. Effects of breastfeeding on the mother. Ped Clin of North America,


2001;48(1):143-5.
2 Horta et al. Evidence on the long-term effects of breastfeeding: systematic reviews and
meta-analysis. Available at www.who.int/child-adolescent-
health/publications/NUTRITION/ISBN_92_4_159523_0.htm. Accessed June 15,
2008.
3 Ip S et al. Breastfeeding and Maternal and Infant Health Outcomes in Developed
Countries, April 2007, Available at www.ahrq.gov/clinic/tp/brfouttp.htm. Accessed
June 15, 2008
4 Becker S, Rutstein S, Labbok M. Estimation of births averted due to breastfeeding and
increases in levels of contraception needed to substitute for breastfeeding, J Biosoc Sci
2003;35:559-574.
5 Huffman, S. L., and Labbok, M. H. (1994) Breastfeeding in family planning programs:
a help or a hindrance? International Journal of Gynaecology and Obstetrics, 47 Suppl,
S23-31; discussion S31-2.
6 Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic
review. Eur J Contracept Reprod Health Care. 2007 Dec;12(4):335-9
7 WHO/UNICEF. Global strategy for Infant and Young Child Feeding, WHO, Geneva,
2003.
8 CDC NIS Survey, infants born in 2005, at
www.cdc.gov/breastfeeding/data/NIS_data/index.htm, accessed August 2008.
9 UNICEF State of the World’s Children 2008
10 Labbok M, Krasovec K: Towards definition of breastfeeding. Stud Fam Plann 21:
226–240, 1990
11 Zinaman MJ, Hughes V, Queenan JT et al: Acute prolactin and oxytocin responses and
milk yield to infant suckling and artificial methods of expression in lactating women.
Pediatrics 89: 437-440, 1992
12 World Health Organization Global Data Bank on Breastfeeding. Geneva: World
Health Organization/United Nations, 1996
13 McNeilly AS: Lactational amenorrhea. Endocrinol Metab Clin North Am 22: 59– 73,
1993
14 McNeilly, A.S. (2001) Lactational control of reproduction. Reproduction, Fertility and
Development, 13(7-8), 583-590.
15 McNeilly AS, Tay CC, Glasier A: Physiological mechanisms underlying lactational
amenorrhea. Ann NY Acad Sci 709: 145–155, 1994
16 Cox D, Owens R, and P Hartmann. Blood and milk. Prolactin and the rate of milk
synthesis in women. Exper Physiol. 1996. 81, 1007-1020.
17 Diaz S, Seron-Ferre M, Croxatto HB et al: Neuroendocrine mechanisms of lactational
infertility in women. Biol Res 28: 155–163, 1995
18 Nunley WC, Urban RJ, Evans WS et al: Preservation of pulsatile luteinizing hormone
release during postpartum lactational amenorrhea. J Clin Endocrinol Metab 73: 629–
636, 1991
19 Zinaman M, Cartledge T, Tomai T et al: Pulsatile GnRH stimulates normal cyclic
ovarian function in amenorrheic lactating postpartum women. J Clin Endocrinol Metab
80: 2088–2093, 1995
20 Kremer JA, Borm G, Schellekens LA et al: Pulsatile secretion of luteinizing hormone
and prolactin in lactating and nonlactating women and the response to naltrexone. J
Clin Endocrinol Metab 72: 294–00, 1991
21 Tay CC, Glasier AF, McNeilly AS: Twenty-four hour patterns of prolactin secretion
during lactation and the relationship to suckling and the resumption of fertility in
breast-feeding women. Hum Reprod 11: 950–955, 1996
22 Diaz, S., Aravena, R., Cardenas, H., Casado, M.E., Miranda, P., Schiappacasse, V., et
al. (1991) Contraceptive efficacy of lactational amenorrhea in urban Chilean women.
Contraception, 43(4), 335-352.
23 Simondon KB, Delaunay V, Diallo A, Elguero E, Simondon F. Lactational amenorrhea
is associated with child age at the time of introduction of complementary food: a
prospective cohort study in rural Senegal, West Africa. Am J Clin Nutr. 2003
Jul;78(1):154-61.
24 Diaz S, Cardenas H, Brandeis A et al: Early difference in the endocrine profile of long
and short lactational amenorrhea. J Clin Endocrinol Metab 72: 196–201, 1991
25 Kurz K, Habicht JP, Rasmussen KM et al: Effects of maternal nutritional status and
maternal energy supplementation on length of postpartum amenorrhea among
Guatemalan women. Am J Clin Nutr 58: 636–642, 1993
26 Wasalathanthri S, Tennekoon KH.Lactational amenorrhea/anovulation and some of
their determinants: a comparison of well-nourished and undernourished women. Fertil
Steril. 2001 Aug;76(2):317-25
27 Neville M: Physiology of lactation. Clin Perinatal 26: 251–279, 1999
28 Rasmussen KM. Association of maternal obesity before conception with poor lactation
performance. Annu Rev Nutr. 2007;27:103-21.
29 WHO Task Force on Methods for the Natural Regulation of Fertility: The WHO
Multinational Study of Breast-feeding and Lactational Amenorrhea: I. Description of
infant feeding patterns and of the return of menses. Fertil Steril 70:448–460, 1998
30 WHO Task Force on Methods for the Natural Regulation of Fertility. The WHO
Multinational Study of Breast-feeding and Lactational Amenorrhea: II. Factors
associated with the length of amenorrhea Fertil Steril 70:461–471, 1998
31 Gray R, Apelo R, Campbell O et al: The return of ovarian function during lactation:
results of studies from the U.S. and the Philippines. In Gray R (ed): Biomedical and
Demographic Determinants of Reproduction, pp 428–445. Oxford: Colorado Press,
1993
32 Diaz S, Cardenas H, Brandeis A et al: Relative contributions of anovulation and luteal
phase defect to the reduced pregnancy rate of breastfeeding women. Fertil Steril
September 58: 498–503, 1992
33 WHO Task Force on Methods for the Natural Regulation of Fertility. The WHO
Multinational Study of Breast-feeding and Lactational Amenorrhea: IV. Postpartum
bleeding and lochia in breastfeeding women. 72:441–447, 1999
34 Perez A, Vela P, Masnick GS et al: First ovulation after childbirth: The effect of
breastfeeding. Am J Obstet Gynecol 114: 1041–1047, 1972
35 Prieto CR, Cardena H, Croxatto HB: Variability of breast sucking, associated milk
transfer and the duration of lactational amenorrhea. J Reprod Fertil 115: 193–200,
1999
36 Kaitz M, Good A, Rohem AM et al: Mother's recognition of the newborns by olfactory
cues. Dev Psychobiol 20: 587–591, 1987
37 Zhu BP, Rolfs RT, Nangle BE et al: Effect of the interval between pregnancies on
perinatal outcomes. N Engl J Med 25;340:589–594, 1999
38 Klerman LV, Cliver SP, Goldenberg RL: The impact of short interpregnancy intervals
on pregnancy outcomes in a low-income population. Am J Public Health 88: 1182–
1185, 1998
39 Rutstein S: Morbidity and mortality outcomes associated with duration of inter-birth
intervals. Unpublished analyses of Demographic and Health Surveys, MACRO,
International, March 2000
40 Farr G, Rivers R: Interactions between intrauterine contraceptive device use and
breastfeeding status at time of insertion: analysis of Tcu-380A acceptors in developing
countries. Am J Obstet Gynecol 167: 144, 1992
41 Nilsson S, Nygren K: Transfer of contraceptive steroids to human milk. Res Reprod
11: 1, 1979
42 Shaaban M, Salem H, Abdullah K: Influence of levonorgestrel contraceptive implants
(Norplant) initiated early postpartum upon lactation and infant growth. Contraception
32: 623, 1985
43 Shaaban M, Olind V, Salem H et al. Levonorgestrel concentration in maternal and
infant serum during use of subnormal levonorgestrel contraceptive implant, Norplant,
by nursing mothers. Contraception 1986, 33:357
44 Massai R, Quinteros E, Reyes MV, Caviedes R, Zepeda A, Montero JC, Croxatto
HBExtended use of a progesterone-releasing vaginal ring in nursing women: a phase II
clinical trial. Contraception. 2005 Nov;72(5):352-7. Epub 2005 Jun 29
45 Hatcher R, Trussell J, Nelson A, et al: Contraceptive Technology, Ardent Media, Inc.
2007, pp 407-409, 759.
46 Diaz S, Zepeda A, Maturana X et al: Fertility regulation in nursing women. IX.
Contraceptive performance, duration of lactation, infant growth, and bleeding patterns
during use of progesterone vaginal rings, progestin-only pills, Norplant implants, and
copper T 380-A intrauterine devices. Contraception 56: 223–232, 1997
47 Diaz S, Reyes MV, Zepeda A et al: Norplant implants and progesterone vaginal rings
do not affect maternal bone turnover and density during lactation and after weaning.
Hum Reprod 14: 2499–2505, 1999
48 Dorea JG, Myazaki ES: Calcium and phosphorus in milk of Brazilian mothers using
oral contraceptives. J Am Coll Nutr 17: 642–646, 1998
49 Dorea JG, Myazaki ES: The effects of oral contraceptive use on iron and copper
concentrations in breast milk. Fertil Steril 72: 297–301, 1999
50 Visness CM, Rivera R: Progestin-only pill use and pill switching during breastfeeding.
Contraception 51: 279–281, 1995
51 Labbok M, Nichols-Johnson V, Valdes-Anderson V. ABM Clinical Protocol #13:
Contraception during breastfeeding, Breastfeeding Medicine 2006;1(1):43-51. Updates
will be available at intervals at
www.bfmed.org/index.asp?menuID=139&firstlevelmenuID=139
52 Tyson JE, Perez, Zanartu J: Human lactational response to oral thyrotropin releasing
hormone. J Clin Endocrinol Metab 43: 760–768, 1976
53 Tyson JE, Freedman RS, Perez A et al: Significance of the secretion of human
prolactin and gonadotrophin for puerperal lactational infertility. Ciba Found Symp:49–
71, 1976
54 Vega RR, Barraza-Vazquez A, Vega MG et al: GnRH agonist for postpartum
contraception: Biochemical, hormonal and endometrial effects. Adv Contracept 12:
15–25, 1996
55 Kennedy K, Rivera R, McNeilly A: Consensus statement on the use of breastfeeding
as a family planning method. Contraception 39: 477–496, 1989
56 Labbok M, Cooney K, Coly S: Guidelines: Breastfeeding, Family Planning, and the
Lactational Amenorrhea Method (LAM). 2nd ed. Washington, DC: Institute for
Reproductive Health, 1994
57 Perez A, Labbok M, Queenan J: Clinical study of the lactational amenorrhea method
for family planning. Lancet 339: 968, 1992
58 Labbok M, Perez A, Valdes V et al: The lactational amenorrhea method: A new
postpartum introductory family planning method with program and policy
implications. Adv Contracept 10: 93– 109, 1994
59 Ramos R, Kennedy KI, Visness CM: Effectiveness of lactational amenorrhoea in
prevention of pregnancy in Manila, the Philippines: Noncomparative prospective trail.
BMJ 12;313:909–912, 1996
60 Kazi A, Kennedy K, Visness CM et al: Effectiveness of the lactational amenorrhea
method in Pakistan. Fertil Steril 64: 717–723, 1995
61 Cooney K, Labbok M et al. An assessment of the nine-month lactational amenorrhea
method (MAMA-9) in Rwanda. Stud Fam Plann 27:102–171, 1996
62 Labbok M, Hight-Laukaran V, Peterson A et al: Multicenter study of the lactational
amenorrhea method (LAM): I. Efficacy, duration, and implications for clinical
application. Contraception 55: 327–336, 1997
63 Hight-Laukaran V, Labbok M, Peterson A et al: Multicenter study of the lactational
amenorrhea method (LAM): II. Acceptability, utility, and policy implications.
Contraception 55: 337–346, 1997
64 WHO Task Force on Methods for the Natural Regulation of Fertility: The WHO
Multinational Study of Breast-feeding and Lactational Amenorrhea. III. Pregnancy
during breastfeeding. Fertil Steril 72:431–440, 1999
65 Peterson A, Labbok M, Hight-L V et al: Multicenter study of the lactational
amenorrhea method (LAM): III. “Post-marketing” study with limited clinical contact.
Contraception 162: 62, 1999
66 Tommaselli G.A., Guida M., Palomba S., Barbato M., and Nappi, C. (2000) Using
complete breastfeeding and lactational amenorrhoea as birth spacing methods.
Contraception, 61(4), 253-257.
67 Shaaban, O.M., and Glasier, A.F. (2008) Pregnancy during breastfeeding in rural
Egypt. Contraception, 77(2008), 350-354.
68 Van der Wijden, C., Kleijnen, J., and Van Den Berk, T. (2008) Lactational amenorrhea
for family planning. Cochrane Database System Review, Issue 4. Art. No.: CD001329.
DOI: 10.1002/14651858.CD001329.
69 Vekemans M: Postpartum contraception: the lactational amenorrhea method, Eur J
Contracept Reprod Health Care 2:105–111, 1997
70 Romero-Gutiérrez G, Vaca-Ortiz N, Ponce-Ponce de León AL, López-Martínez
MG.Actual use of the lactational amenorrhoea method.Eur J Contracept Reprod Health
Care. 2007 Dec;12(4):340-4.
71 Zhang, L. Y., Liu, Y. R., Shah, I. H., Tian, K. W., and Zhang, L. H. (2002)
Breastfeeding, amenorrhea and contraceptive practice among postpartum women in
Zibo, China. European Journal of Contraception and Reproductive Health Care, 7(3),
121–126.
72 Hardy D, Santos LC, Osis MJ et al: Contraceptive use and pregnancy before and after
introducing lactational amenorrhea (LAM) in a postpartum program. Adv
Contraception 14: 59– 68, 1998
73 Hight-Laukaran, V., Rutstein, S. O., Labbok, M. H., and Ballard, E. (1996)
Contraceptive use during lactational amenorrhea. International Journal of Gynaecology
and Obstetrics, 54(2), 101–108.
74 Lopez-Martinez M, Romero-Gutierrez G, Ponce-Ponce De Leon A. (2006.)Acceptance
of lactational amenorrhoea for family planning after postpartum counseling. The
European Journal of Contraception and Reproductive Health Care, 11(4), 297-301.
75 Vural, B., Vural, F., Erk, A., and Karabacak, O. (1999) Knowledge of lactational
amenorrhea and contraception in Kocaeli, Turkey. East African Medical Journal,
76(7), 385–389.
76 Khella, A. K., Fahim, H. I., Issa, A. H., Sokal, D. C., and Gadalla, M. A. (2004)
Lactational amenorrhea as a method of family planning in Egypt. Contraception, 69(4),
317–222.
77 Kennedy, K.I., Kotelchuck, M. (1998) Policy considerations for the introduction and
promotion of the lactational amenorrhea method: Advantages and disadvantages of
LAM. Journal of Human Lactation, 14 (3), 191-203.
78 Kennedy, K.I., Kotelchuck, M., Visness, C.M., Kazi, A., & Ramos, R. (1998.) Users’
understanding of the lactational amenorrhea method and the occurrence of pregnancy.
Journal of Human Lactation, 14 (3), 209-218.
79 Van der Wijden C, Kliejnen J, Ven Den Berk T. Lactational amenorrhea for family
planning. Cochrane Database System Review, issue 4. Art. No. CD001329, 2008.
80 American Academy of Pediatrics Statement on Breastfeeding, 1999
81 WHO/UNICEF. Global Strategy for Infant and Young Child Feeding. WHO, Geneva,
2003.
82 Cohen R, Brown KH, Canahuati J et al: Effects of age of introduction of
complementary foods on infant breast milk intake, total energy intake, and growth: a
randomised intervention study in Honduras. Lancet 344: 288–293, 1994
83 Dewey KG, Cohen RJ, Rivera LL et al: Effects of age at introduction of
complementary foods to breast-fed infants on duration of lactational amenorrhea in
Honduran women. Am J Clin Nutr 65: 1403–1409, 1997
84 Bongiovanni, A., Samam’h, M.A., Al’Sarabi, R.H., Masri, S.D., Zehner, E.R., and
Huffman, S.L. (2005) Promoting the Lactational Amenorrhea Method (LAM) in
Jordan increases modern contraception use in the extended postpartum period. The
Linkages Project. Washington, DC: Academy for Educational Development.
www.linkagesproject.org/media/publications/LAM%20Research%20Report,%20Final,
%20November%201,%202005.pdf
85 Ford K, Labbok M: Breast-feeding and child health in the United States. J Biosoc Sci
25: 187–194, 1993
86 Afifi, M. (2007) Lactational amenorrhoea method for family planning and women
empowerment in Egypt. Singapore Medical Journal, 48(8), 758-762.
87 Wiley AS: The ecology of low natural fertility in Ladakh. J Biosoc Sci 30: 457–480,
1998

View publication stats

You might also like