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May I just comment on history? The first described case of artificial feeding was by one of the Assyrian kings. Also, in archaeological investigations of cultures along the Indus, many spoons and feeding utensils that were obviously used for artificial feeding have been found. So all through history this has been common. In Sweden in 70 and 150 A.D. there were areas where there was no breastfeeding at all; nobody knows why. And there was a law in Norway from 1040 that mothers should breastfeed, obviously, because of the fact that many didn't, so this is an old thing.
I would like to explore a little more with you and Dr. Woolridge the issue of women feeling that they have insufficient milk. This seems to come out of every culture that we've heard about today, and, certainly, my experience in Africa is similar. Women will say that they are worried that they don't have enough milk. Where formula or other foods are available, they'll move on to either. What is it that women expect of a baby that makes them feel that they don't have enough milk? Dr. Woolridge showed that a lot of perceived milk insufficiency is found in women with milk volume in the normal range. From my own experience, having breastfed in the United Kingdom and in Africa, British women expect children to stay asleep for long periods at night. The family expects it even if the mother doesn't, which puts a lot of pressure on women to somehow make the child not feed at such frequent intervals. I just wondered if similar sorts of cultural problems would be underlying your women's responses as well?
I think the infant's behaviour often raises the question of whether milk production is sufficient. It is not the same in rural areas, where the infants probably cry as much as urban infants, but they don't have any other option.
Our rural mothers may breastfeed 20 times a day. In the waiting room, they feed once, twice, or three times. When you ask them how many times they have breastfed today, they say maybe one, two, or five times, but they don't have this notion that taking the baby to the breast often is a bother. But for mothers from higher socio-economic groups, if the baby is not quiet for four hours, which was what they were used to when the babies were bottle-fed, they feel they don't have milk.
I think there is a total difference in outlook between a mother in the United Kingdom and a mother in Thailand. As we have just heard, the mothers in Thailand have no expectation of failing. They just assume it is the only option, and they will do it successfully. Intriguingly, they still report perceptions of insufficient milk, but it doesn't cause them to discontinue breastfeeding. It is a common cultural concern, even in that sort of society. I agree that in the United Kingdom there is an expectation that a baby should sleep for long stretches to fit in with the adult lifestyle. It's an inappropriate expectation, and much of it has been derived from formula-feeding.
Mary Houston investigated this question of insufficient milk. She concluded that for many women it was a legitimate reason for giving up breastfeeding. If a woman says she doesn't have enough milk, she shouldn't carry on, because it's going to damage the child. Some women were certainly using that as a legitimate excuse to stop breastfeeding.
I think that is true for our urban group. As you could see, the individual who most often bought the first can of formula without any advice was the mother. She was really legitimizing her decision to stop breastfeeding by saying that she had insufficient milk production.
Dr. Van Eskrik
If I may comment on the Thai example, different methods produce very different pictures. I was doing ethnographic work in another part of Thailand, and the discussions about insufficient milk were quite different. Of course, they are not phrased that way, but I came across two things quite regularly, not in questioning but from observation. First, women were becoming concerned that their breasts were too small, that there was something wrong with their shape. There are pictures on calendars in every tiny hut, and a woman would be very strongly influenced to think about whether or not her breasts were adequate to this task. That's something that I think is changing quite rapidly. The second is a fundamental approach, strongly linked with Theravada Buddhism, that the capacity to nurture well is a result of merit stored from former lives. This means that women talk about themselves as being someone who is either a good nurser or not a good nurser, almost as if we would say that this is a characteristic that they would expect to see in themselves. It is also very interesting to think about how women classify themselves as both mothers and women. I know it doesn't fit with the kind of work you were doing, but at least it suggests perhaps another way to look at cultural factors.
May I make a point about almost a war of communication that seems to be a common factor in developed and developing countries? I think one of your slides made the point how clever formula manufacturers are at getting their message across. In fact, they target health professionals even more than they target the patients themselves, and how successful that campaign is! We have seen literature distributed by the manufacturers who now have an obligation to state the advantages of breastfeeding. They give one page on the benefits of breastfeeding and maybe five pages about cracked nipples, tiredness, and breast abscess. In fact, the section that is supposed to encourage breastfeeding mothers is targeted so cleverly that it has exactly the opposite effect. What do you feel about making a systematic attempt to get better education that is not dominated by the formula manufacturers, so that some misunderstandings about breastfeeding can be overcome? We recently asked mothers who were breastfeeding if they knew that the baby would lose weight in the first few days after birth, and the number who knew this was about 5%. We are simply not getting basic information over to our mothers, and I suspect from what you are saying that there is a failure in Mexico, the United Kingdom, and many other countries.
There are two sides to this problem. One is to attack the problem of medical education by working with assistant professors of paediatrics who are lecturing to students, inviting them to seminars about lactation and so forth. This is a huge task. The other is the lack of a strong network of people promoting breastfeeding awareness to hospitals, physicians, and the general public to counteract the propaganda from formula manufacturers, because most literature handed to mothers is prepared by those companies.
What is more comfortable for a working mother three months after the child's birth, breastfeeding or bottlefeeding, and why?
I would say breastfeeding. The situation, though, is that we put so many obstacles against mothers breastfeeding successfully that we have this notion that the mother and baby have to be changed to fit the circumstances of work and so forth. We shouldn't be changing human behaviour, we should be changing working conditions to fit breastfeeding.
Many years ago the labour laws in Mexico supported long post-partum leaves of absence intended to aid breastfeeding. However, fewer than half of the mothers breastfed for such a long period, so the outcome was the reverse of what many expected.
Let me put it another way, that convenience is in the eye of the beholder. If you do a survey in the United States, uppereconomic-class women will tell you that breastfeeding is by far the most convenient, for all of the reasons we know. If you ask lower-economic-class women the same question, you don't get the same answer. Their lives are chaotic, they're on the bus, they're embarrassed to breastfeed on the bus. The last thing in the world they consider breastfeeding to be is convenient for them. The answer to Dr. Perez's question depends on a woman's life circumstances, and whether breastfeeding works for her. It's wonderful to have labour laws to say you're entitled to a maternity leave, and if you have a job or are protected by these laws, that may be wonderful in other ways. The United States is in the embarrassing position of not even having such laws, so I can hardly cast any stones. What about women who work in the informal sector for whom there is no protection whatsoever? Their labour is just as valuable to their families, the interference of their work conditions with breastfeeding may be as great or greater, yet they have no protection at all. In their case, convenience, again, may be an issue.
We are researching that area. We have a study on working women, and one aspect we are concerned about is women's satisfaction with breastfeeding. We were surprised that the mothers in the control group who did not breastfeed were very satisfied, and the mothers who exclusively breastfed or human-milk-fed for six months, even while working, were equally satisfied.
I use the Swedish example, where it is rare for mothers not to breastfeed. They are entitled to 18 months off, most of that period with full pay, so it works.
To go back to the issue of insufficient milk and mothers' perceptions, I think many women don't understand lactation well. They are encouraged to think that their milk will come in and their breasts will feel very full. But at about four to six weeks the breast physiologically adapts, so that they have less fullness and enlargement. Some women interpret the change in sensation to mean that they have less milk. They really need to understand that lactation is an adaptive process, and even though the breasts are quite soft, they still produce milk.
One issue I don't think is covered much in connection with the insufficient-milk syndrome is the contribution that the infant makes to the mother's perception about insufficient milk. We have to remember that the infant regulates its intake by many different aspects of its sucking behaviour. To a large extent, this is accomplished by differences in sucking amplitude or frequency. The infant has some degree of control over what actually takes place. We seldom look at the contribution the infant makes to the mother's decisions regarding feeding.
This also extends to another comment I want to make in connection with the determinants of milk production. There is an enormous variability in birthweight in different populations in the world. In Sweden, for example, the average is approximately 3,500 g. In Santa Maria Cauque, Guatemala, the average is approximately 2,600 g, a 900-g difference. There is likely a relation between an infant's birthweight and its sucking behaviour. The degree of breastfeeding success in different populations is also determined, in part, by other infant characteristics. Yet in general, there tends to be a greater emphasis placed on the mother as the one who will make the final decisions on what is going to happen, and not enough attention is given to the infant's roles.
Let me go back to the role the infant plays, because I think it is an important one. In studies we did about 10 years ago, we were interested in understanding whether infants were hungry whenever they demonstrated behaviours that the mother interpreted as hunger. We followed women longitudinally for four months beginning at about the third month postpartum. Women who were planning to breastfeed for 6 to 12 months were recruited. At the point they introduced solid foods, we asked why they were doing this. I think 100% of them said it was because the child was either fussy or not sleeping. They were interpreting this as evidence that the child was hungry and, therefore, that they were unable to sustain or increase milk production sufficiently to satisfy the infant.
The remarkable thing, however, was that when we measured the energy consumption of infants before and after the introduction of solid foods, we found no difference. Thus, I think children give certain cues that women interpret as hunger but that are, in fact, driven behaviourally by other needs. The child likely has reached the point where it wants to put something else in its mouth, and mothers tend to interpret those cues as hunger. Because the infant's behavioural response to other foods is often positive, their mistaken interpretations are reinforced. In fact, those responses appear to have nothing to do with physiological hunger defined in the usual terms. There are inappropriate periods in early infancy to introduce other foods. The physiological timing of complementary foods determined by behaviours other than hunger is dependent on a number of conditions that relate to the infant's surroundings.
Studies have investigated infant intake by 24-hour test weighings. Fewer than 50% of suckling episodes result in the intake of more than 50 g of milk. The remainder result in the intake of as little as 5 or 10 g of milk. This suggests that the infant is not really hungry. It's just sucking for the joy of sucking.
I would like to return to the determinants of a woman's preference, because I cannot understand why generally in Latin America, fewer than 20% of women are fully breastfeeding at six months post-partum? We need to find an answer to that.
I haven't heard anybody talk about the same woman with different babies in successive births. Is past behaviour predictive of future behaviour?
We did research on that. Some mothers who tended to breastfeed one child for a long time were likely to do the same with the next child. If mothers breastfed a very short time, the results were about the same in subsequent pregnancies. There was, however, a gray area when mothers breastfed from one to six or seven months. They were very unpredictable. One could not predict what would happen with the next baby.
I would like to go back to a point raised earlier. I think babies have very strong personalities. When we did our pacifier study, the main factor influencing pacifier use was the infant. Some babies just refuse them, and those are the babies who tend to breastfeed longest.
To add a caveat to that, in our African experience, where 100% of women were breastfeeding for 18 months or so, women in successive lactations tended to show a characteristic breastmilk volume and breastmilk composition. Thus, it's a mixture of culture, maternal feelings, and the way a mother's breasts work.
Alan S. McNeilly
Breastfeeding suppresses fertility for a variable length of time, but when certain criteria are applied, it can be a reliable contraceptive. The individual variation in duration of infertility is directly related to suckling activity. As suckling declines, follicle growth resumes and ovulation may occur. Infertility is maintained by suckling-induced disruption of the normal pattern of pulsatile luteinizing hormone release and is related to an increased sensitivity of the hypothalamus to the negative feedback effects of oestradiol. Even if ovulation does resume, the corpus luteum function is often insufficient to maintain pregnancy. Attempts to alter suckling activity to prolong lactational infertility are not successful, but maintenance of reasonable suckling frequencies of normal duration can protect women from pregnancy for a prolonged period postpartum.
It is quite clear that breastfeeding results in a suppression of fertility for a prolonged period of time, depending on the pattern of suckling behaviour [1-3]. Stimulation of the nipple during suckling results in three responses: first, the release of oxytocin from the posterior pituitary to allow release of the milk present in the breast to the baby; second, the release of prolactin, which is essential for milk production for the subsequent feeding; and third, the suppression of gonadotrophin secretion, which results in suppression of ovarian activity. When established, the pattern of suckling varies considerably, and this is dependent on the mother and child and is not necessarily controllable. Throughout lactation, the duration of lactation and the duration of infertility are directly related to the suckling pattern. Attempts to increase suckling frequency to maintain longer durations of amenorrhoea have not been successful, because the mother and the baby interact so that the amount of nutrition received by the baby remains fairly constant . As suckling frequency is artificially increased above that established in lactation, there is a concomitant decrease in suckling duration at each feeding. Thus, the overall duration and intensity of suckling remain the same, and there is no overall effect on the duration of infertility. It is, therefore, important to understand all the different components of suckling that relate to the suppression of fertility, and these have been reviewed in detail recently [2, 3, 5]. This article briefly reviews the present state of knowledge regarding the principal mechanisms involved in suckling-induced infertility.
Ovarian activity and the interbirth interval
The components of the interbirth interval are important to understand before any discussion of the control of gonadotrophin secretion during lactation. The interbirth interval consists of four periods: (1) the recovery from pregnancy; (2) a period of amenorrhoea during breastfeeding; (3) the resumption of the ovulatory cycles (which may not take place if a new conception occurs); and (4) finally, a new pregnancy. Over a number of years, we have investigated the interactions between the suckling pattern and the resumption of ovarian activity in relation to the pattern of gonadotrophin secretion. In some women, where suckling is maintained at a high level, ovarian steroid secretion can be suppressed for a number of months and even years, even in well-nourished Western societies . In other women, where suckling frequency is lower, ovarian activity will resume earlier. In Edinburgh it was shown that if the frequency of suckling is maintained above five times a day and the duration is maintained above 65 minutes a day, amenorrhoea will often be the consequence . Although the exact frequency and duration of suckling required to maintain infertility vary among societies, it is usually possible to establish a guide for the suckling required .
During the period of lactational amenorrhoea, the plasma concentrations of oestradiol secreted by the dominant follicle(s) remain minimal, in contrast to the normal increase seen during the follicular phase of the normal menstrual cycle [2, 3]. These results suggest that there is minimal ovarian activity, as follicle development during the normal menstrual cycle is always associated with an increase in oestrogen secretion. During early lactation (up to 12 weeks post-partum), ultrasound visualization of the ovary confirmed the absence of follicle development . At later stages in lactational amenorrhoea, however, although oestrogen secretion remained minimal, follicles up to preovulatory size (around 20 mm diameter) were detected by ultrasound . The reason for the presence of follicles that secrete low amounts of oestrogen relates to the effect of suckling on the secretion of the gonadotrophins luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The low steroid-secreting activity of these follicles presumably relates to a reduced input of gonadotrophin, particularly of LH. This possibility will now be discussed.
Changes in FSH and LH
During the menstrual cycle, a rise in plasma FSH at the beginning of the cycle stimulates the growth of a cohort of follicles, which increase to around 10 mm in diameter by the mid-follicular phase. At this stage, a single follicle continues to grow up to around 20 mm in diameter, becoming the preovulatory follicle that will ovulate. The selection of this dominant follicle is dependent on a fall in the plasma concentration of FSH occurring about days 6 to 8 of the follicular phase. As the follicle grows, it acquires the ability to secrete oestradiol by conversion of androgen from the outer thecal layer of the follicle to oestradiol by the granulosa cells within the follicle. Only LH, released in pulses, stimulates thecal androgen production. FSH alone does not stimulate steroid secretion from the ovary. The increase in plasma oestradiol secreted by the developing preovulatory follicle leads to positive feedback and the discharge of the preovulatory surge of LH. This induces ovulation, luteinization of the follicle, and formation of the corpus luteum, which secretes progesterone in response to a slow pulsatile secretion of LH. The progesterone and oestradiol released by the corpus luteum decrease the pulse frequency of release of gonadotrophin-releasing hormone (GnRH) from the hypothalamus, which drives the pulsatile release of LH from the pituitary. The decline in GnRH pulsatile stimulation, together with inhibin A released from the corpus luteum, leads to a major suppression of release of FSH and an inhibition of follicle development during the luteal phase. If conception does not occur, the corpus luteum regresses and the resulting drop in steroid and inhibin concentrations results in an increase in FSH that initiates the next wave of follicle development. These events are all closely coordinated and regulated by the rate of pulsatile secretion of GnRH from the hypothalamus, which stimulates the pulsatile release of LH. During the follicular phase of the normal menstrual cycle, the GnRH/LH pulse frequency increases to around one pulse per hour, and any disruption or slowing in the pulsatile release of GnRH/LH prevents normal follicle development and reduces steroid secretion by the developing follicle.
During breastfeeding the plasma concentrations of FSH increase rapidly after birth. By four weeks post-partum, they are within the normal early follicular range, whether or not breastfeeding occurs . These levels of FSH are maintained throughout the duration of lactational amenorrhoea and are substantially higher than those seen during the luteal phase of normal cycles. Thus, any apparent absence of follicular development associated with low oestrogen secretion cannot be due to lack of FSH. Indeed, it is probable that this maintained high level of FSH is the cause of the observed growth of follicles up to the preovulatory level. The low steroid secretion must relate to the difference in pattern of LH secretion.
The pattern of 24-hour profiles of LH secretion at four weeks post-partum is very variable. Most women show no evidence of pulsatile secretion of LH, whereas in some there is a resumption of LH pulsatile secretion. But this occurs at random and at a slow frequency . In some women with slow pulsatile LH secretion, pulsatile release of FSH is also seen, a rare occurrence in the normal menstrual cycle that is related to the very low levels of oestrogen and inhibin released from the inactive ovary. As the pulse frequency of LH secretion increases, the pulsatile release of FSH is lost, and a natural pattern of FSH secretion similar to that in the normal cycle resumes. Thus, FSH pulses may occur, but only when the negative feedback from the ovary is suppressed. After four weeks there is a gradual increase in the frequency of pulses of LH, but for many weeks, particularly during lactational amenorrhoea, the pulse frequency remains erratic and below the normal follicular phase frequency required to stimulate normal oestradiol secretion from any developing follicle. Thus, although the plasma levels of FSH are sufficient to stimulate follicle development as seen by ultrasound, the suckling stimulus prevents the resumption of a normal frequency of pulsatile LH secretion, and the follicles make only limited amounts of oestradiol. The rate of return of normal pulsatile secretion is very variable among women, and it is this variation that causes the variation in the resumption of fertility. It is presumed that the variability is due to the differences in the patterns and intensity of suckling, and that this is why it is difficult to control.
The disturbance in the pattern of pulsatile LH release is almost certainly the cause of the lack of oestrogen secretion by follicles, resulting in a lack of ovulation. In a study in which GnRH pulses were replaced at the normal follicular phase frequency of once per 60 minutes in breastfeeding women at six weeks post-partum, at a time when ovarian activity was completely suppressed as indicated both by oestrogen and by ultrasound, normal pre-ovulatory follicle growth and oestrogen secretion were induced without a problem . Ovulation occurred, although this was followed by an inadequate corpus luteum. When the pump was turned off and GnRH infusion stopped, ovarian activity was suppressed for at least 10 weeks in most women. Thus, restoring a natural, follicular-phase pattern of pulsatile GnRH secretion in breastfeeding women will induce the growth of normal pre-ovulatory follicles, indicating that the aberrant pattern of LH secretion during lactational amenorrhoea causes the failure of normal oestrogen secretion. Therefore, no pre-ovulatory LH surge would be induced, owing to the lack of oestrogen-positive feedback, and ovulation would not occur. Prolactin and suckling remained high throughout the period of GnRH pulsatile infusion between 6 and 10 weeks post-partum, showing that there was no direct interference of prolactin with gonadotrophin action at the ovarian level.
The mechanism by which suckling interferes with the normal pattern of GnRH release is unclear. The potential role for endorphins acting in the hypothalamus has been discussed elsewhere [3,12]. Infusion of the opiate antagonist naloxone failed to increase the secretion of LH and FSH in a significant manner in normal breastfeeding women . Nevertheless, in women receiving the progesterone-only birth control pill, a small increase in LH and FSH release did occur. This could be expected, as the negative feedback effect of progesterone on GnRH pulsatile secretion during the luteal phase of the menstrual cycle is thought to be mediated by an increase in opiate tone within the hypothalamus. One interesting observation was that treatment with an opiate antagonist increased the amount of LH and FSH released in response to GnRH. At the present time, there is no explanation for this effect, because no opiate receptors have been described in the pituitary gland. It may be that the opiate tone is so high in the hypothalamus that we are unable to give sufficient opiate blocker to affect the system. Because of passage of the blockers to the infant through the breastmilk, however, it would be unethical to use higher doses than we originally used. Thus, a role for endorphins in the suckling-induced disruption of GnRH release remains unproven in women.
There is one final aspect of the control of GnRH release, and hence of LH and FSH release, which is very important. Treating breastfeeding and bottle-feeding women with oestrogen at different times during the return of fertility during lactation showed clearly that there was an increase in sensitivity to the negative feedback effects of oestrogen on LH and FSH secretion and a failure of positive feedback, leading to a failure of oestrogen to induce the pre-ovulatory surge of LH . We have now shown that breastfeeding women are hypersensitive to oestrogen: the use of transdermal patches to increase plasma concentrations of oestradiol to early follicular phase levels results in a rapid inhibition of further pulsatile release of LH, attributable to an inhibition of GnRH release from the hypothalamus . This could be crucial in our understanding of how suckling suppresses fertility, although the mechanisms are unknown. The increased sensitivity to oestrogen must be induced by suckling, because in breastfeeding women who wean their babies, there is an early return to the normal feedback sensitivity to oestrogen. The implications are that when the levels of FSH are sufficient to initiate and maintain the growth of large follicles, the slow pulse frequency of LH caused by the suckling stimulus is only sufficient to allow these follicles to release small amounts of oestradiol. However, the increase in sensitivity of the GnRH pulse generator to oestradiol means that the small amount of oestradiol released from the follicle will be sufficient to switch off further GnRH/LH release, and the follicle will stop making oestradiol. Thus, no pre-ovulatory LH surge will be generated, and ovulation will not occur. If suckling was rapidly cut down around this time, then the increased sensitivity of the GnRH pulse generator would disappear, a pre-ovulatory LH surge could be induced, and ovulation and pregnancy could occur without any major warning during lactational amenorrhoea. This is rare but does occur .
Plasma concentrations of prolactin decline during lactation, even though suckling is maintained. The amount of prolactin released during suckling declines with time, but each suckling episode is associated with an increase in prolactin, even though this may be small. The amount of prolactin released during the afternoon appears to be greater than in the morning, and this has recently being confirmed by 24-hour profiles of prolactin release [11, 16]. It is quite clear that early in breastfeeding, by four weeks post-partum, the normal increase in prolactin associated with sleep that occurs during the normal menstrual cycle resumes, and superimposed upon this is the prolactin response to suckling. The amount of prolactin released during suckling at night appears to be greater than that released during the day, but the pattern is very variable. By eight weeks, the amount of prolactin released over the 24hour period has declined, but every suckling episode still releases prolactin. The pattern of prolactin release is entirely dependent on suckling. In a woman feeding six to eight times a day, each suckling episode is normally associated with an increase in prolactin, followed by a decline almost down to baseline, provided the next suckling episode does not occur within two hours. If, however, suckling is very frequent, then prolactin levels do not decline between suckling episodes and high levels of prolactin are maintained. Only when suckling is stopped (for instance, during sleep) does the prolactin concentration decline, but as soon as suckling recurs at a high frequency, prolactin levels increase and are maintained high. The release of prolactin in response to suckling does not appear to be related to opiates, because infusion of the opiate receptor blocker naloxone does not influence the amount of prolactin released in response to suckling. In contrast, dopamine clearly suppresses prolactin release, even during lactation when prolactin levels are high. The dopamine receptor blocker metaclopramide causes a huge release of prolactin, 10- to 70-fold higher than that induced by suckling, showing that during lactation, dopamine still maintains a tight control on prolactin release.
Whether the high plasma concentrations of prolactin maintained throughout lactation are part of the mechanism through which suckling suppresses GnRH/LH release is unclear. Dopamine is the principal regulator of prolactin secretion, acting directly on the pituitary lactotrophs to suppress prolactin release. It has been shown in a few species that prolactin can regulate its own secretion by directly increasing dopaminergic tone and dopamine release from the hypothalamus, and dopamine can suppress GnRH release . Nevertheless, blocking dopamine receptors with the dopamine antagonist metaclopramide at 12 weeks post-partum in fully breastfeeding women did not affect LH or FSH secretion or the pituitary responsiveness to GnRH, even though the treatment caused a massive release of prolactin, indicating that it was indeed active . Thus, it appears that dopamine itself does not directly control the pattern of pulsatile GnRH release.
The interaction between prolactin and GnRH release is clearly important, because patients with pathological hyperprolactinaemia often have amenorrhoea and a disrupted pattern of LH/GnRH release . Thus, it is tempting to assume that the high levels of prolactin associated with lactation suppress LH and FSH release, presumably by affecting GnRH release. Previous studies have indicated a reasonably close association between the number of subjects with high levels of prolactin and the duration of lactational amenorrhoea [for example, 1820]. Indeed, one study showed that women who have an increased release of prolactin in response to suckling have a longer duration of amenorrhoca [21, 22]. Nevertheless, in our own studies over a number of years, we have been unable to show any close association between the amount of prolactin released, the pattern of prolactin release, and gonadotrophin secretion. Indeed, over a 24-hour period, pulsatile secretion of LH often coincides with times of maximum prolactin secretion during suckling, particularly when the prolactin response to suckling is highest at night [16, 17]. Equally, it is clear that the pattern of return of GnRH pulsatile release is not like that in puberty, when maximum pulsatile release of LH occurs during sleep. It is possible that the effect of prolactin is very subtle and relies on the plasma concentrations of prolactin remaining above an inhibitory threshold, which would suppress the normal pattern of GnRH release. It is not clear how this threshold could be assessed, but in previous studies it was observed that women had variable basal plasma concentrations of prolactin during normal menstrual cycles after weaning (Howie PW, McNeilly AS, unpublished observations, 1983). These prolactin levels could differ by up to fourfold. During lactational amenorrhoea in these women, the level of prolactin below which ovarian activity resumed related directly to the level of prolactin during the menstrual cycle in the individual woman. More work is required to determine whether prolactin plays a major role in suppressing GnRH output, but it is clear that the pattern of prolactin secretion is directly related to the pattern of suckling. How suckling influences GnRH and, hence, gonadotrophin secretion remains unclear .
The foregoing discussion has made it clear that suckling is the key to the suppression of fertility. The variable return of ovarian activity is related to the variable pattern of suckling input and how fast the baby feeds. It is known that conception rates in women who are still breastfeeding but have resumed menstrual cycles are lower than those in women who have resumed menstruation after stopping contraception. The reason for this has now become clear. When ovulation occurs during lactation, it is often associated with reduced or inadequate corpus luteum function, resulting in reduced progesterone secretion [23-25]. The implication is that conception in a number of cycles can occur, but inadequate luteal function prevents continuation of the pregnancy. In some women menstruation does not resume before the return of full fertility. The first ovulation is normal, and pregnancy may occur without a preceding menstrual period. This, however, is rare and in our experience is related to a rapid reduction in suckling input. The cause of this inadequate corpus luteum function is still not absolutely clear. In bottle-feeding women, the first menstrual cycle is often associated with inadequate luteal function, and this has been related to a reduction in the amount of LH released during the pre-ovulatory LH surge . A similar situation may occur during breastfeeding, and as luteal function improves during subsequent ovulations, the amount of LH released during the pre-ovulatory surge also increases .
Suckling interferes with GnRH secretion early in lactation by disrupting the pattern of GnRH release, so that it does not occur at a constant rate of once every 60 to 90 minutes, the normal pattern seen during the follicular phase of the cycle. FSH levels are high, so follicles can develop, but oestrogen secretion is compromised by this inadequate LH input. As suckling declines, the pattern of GnRH release becomes more constant, and this relates to the increase in oestrogen secretion seen during the later part of lactation. Nevertheless, when this follicle discharges an LH surge to induce ovulation, the following luteal function may not be normal. This may be related to a decrease in the amount of GnRH released during the pre-ovulatory LH surge and the altered sensitivity to positive feedback caused by oestrogen. Only when weaning is almost complete does one normally see the resumption of normal ovarian activity in ovulatory cycles.
Suckling is the interaction between the baby and the mother, and this interaction is crucial to the suppression of fertility. The suppression of fertility is associated not with a complete suppression, but with a disrupted pattern, of GnRH pulsatile secretion. Whether prolactin is involved remains unresolved. Although the exact mechanisms by which breastfeeding suppresses fertility are not known, it is clear that suckling activity is the major controller of the duration of infertility.
It is a pleasure to acknowledge my colleagues Peter Illingworth, Peter Howie, Anna Glasier, and Clem Tay for all their help during these studies.
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