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Department of Nutritional Sciences, University of Connecticut, Storrs CT 06269-4017
3To whom correspondence should be addressed. E-mail: rperez{at}canr.uconn.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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KEY WORDS: • breastfeeding • lactogenesis stage II • perceived onset of lactation • validity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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, 2
). The gold standard for measuring LS-II is test
weighing the newborn before and after each feeding to measure milk
intake and to determine the point in time at which there is a sudden
increase in the slope of the milk volume (MV) curve (1
, 2
).
Some researchers have used breast milk biomarkers (BMB), such as
citrate and lactose, to determine when LS-II occurs
(3
). Researchers have also used maternal perception of the
onset of lactation (OL) as a proxy for LS-II (4
). This
is an attractive low cost method for public health purposes because it
is noninvasive and quick. Furthermore, it is based on the sensations of
a mother that may influence infant-feeding decisions. There are,
however, a number of questions that need to be addressed regarding the
validity and public health meaning of OL. Thus, the objectives of this
article were to answer the following questions: 1) Is OL a
valid proxy of LS-II?, 2) When does OL occur?, 3)
What cues do women use to identify OL?, 4) What MV is
transferred to the infant when women report OL?, 5) Can
women recall the timing of OL when interviewed months after delivery?,
and 6) What are the public health implications of delayed
OL? |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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–15
) (Hilson, J. and Rasmussen, K., personal
communication). The key words used for the MEDLINE search were: human
lactogenesis, OL and MV with or without including specific
researchers’ last names. Studies were included if they: assessed OL
and/or determined LS-II based on milk transfer and/or BMB. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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BMB (3
, 8
) and MV (11
) studies indicate that
OL occurs 12–24 h after LS-II has begun. Thus, researchers have
concluded that OL may not be a valid indicator of LS-II
(3
). This reasoning, however, can be questioned on two
fronts. First, if women tend to systematically report OL later than
LS-II, then OL may be a useful marker for LS-II. Second, women
are more likely to make infant-feeding decisions based on their
perceptions and not on imperceptible changes in BMB or MV.
Prospective studies assessing risk factors for delayed LS-II that
have used multiple markers of LS-II including OL have shown a
remarkable consistency in the conclusions reached regardless of marker
used. A study conducted in Australia (3
) found a
significant delay in LS-II associated with insulin-dependent
diabetes mellitus (IDDM) when BMB or OL was used. This delay was
19 h based on the end of the lactose transitional period, 12 h based on the end of the citrate transitional period, 7 h based
on the beginning of the citrate transitional period, and 26 h
based on OL. The correlation coefficients between MV and BMBs ranged
from 0.47 to 0.69 (P < 0.001). Likewise, a Connecticut
study (9
) found that women with IDDM had an OL delay of
23.8 h (P < 0.05), compared with a reference
group who delivered vaginally. The difference in OL between IDDM women
and the control group matched for Cesarean section deliveries was of
6 h (P > 0.05). These differences were 15.1 and
5.0 h, respectively, defining LS-II as the point at which the
milk lactose and total nitrogen concentration curves intersected
(8
). MV results were fully consistent with BMB and OL, and
the correlation between MV and breast milk lactose concentration at d 7
postpartum was r = 0.57–0.68 (8
).
In agreement with the study by Ferris et al. (9
), several
(5
, 6
, 12
), but not all (10
, 16
), studies have
identified Cesarean sections as a significant risk factor delaying OL
from 7 to 24 h. A recent study by Chapman and
Pérez-Escamilla (5
) may explain inconsistencies
across studies because it found that emergency but not scheduled
Cesarean sections were a risk factor for delayed OL, compared with
vaginal deliveries.
A study in Davis, California (7
) found, among women
delivering vaginally, that primiparous women had an OL 35 h later
than their multiparous counterparts. Consistent with this finding,
infants from primiparous women consumed 194 mL less breast milk at d 5
postpartum. Milk casein and lactose appearance followed the same
pattern of association, suggesting delayed LS-II among primiparous
women, but differences did not reach statistical significance.
Prospective studies conducted in the United States (5
, 6
)
(Hilson, J. and Rasmussen, K., personal communication) also found
significant (P < 0.05) 10- to 14-h delays
in OL associated with primiparity (Table 1
).
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) identified maternal exhaustion soon after
delivery as a risk factor for delayed lactogenesis regardless of marker
used: OL, MV or BMB. Correlation coefficients of four stress indicators
(umbilical cord cortisol and glucose concentration, duration of second
stage of labor and maternal exhaustion soon after delivery) with OL
(r = 0.37–0.63) were of similar magnitude as those
with MV (r = -0.37 to -0.44) or breast milk casein
appearance (r = 0.35–0.65). Furthermore, the
correlation between breast milk consumption at d 5 and OL was
r = -0.60, and between casein appearance and OL was
r = 0.49 (P < 0.0001 in both
instances). In full agreement with these stress findings, Chapman and
Pérez-Escamilla (5
) found that the association
between primiparity and delayed OL was explained by a longer duration
of labor among primiparous than among multiparous women. Furthermore,
vaginal deliveries with longer stage 2 labor duration and women with
emergency, but not scheduled, Cesarean sections were at significantly
higher risk of experiencing a delayed OL than women who had vaginal
deliveries with relatively short durations of the second stage of
labor. In Guatemala (16
), multiparous women without
delayed OL (i.e., 
72 h postpartum) had significantly lower
salivary cortisol concentrations than those with a delayed OL (0.668
± 0.556 µg/dL vs. 0.859 ± 0.505 µg/dL; P
= 0.001).
Chapman and Pérez-Escamilla (4
) recently tested the
validity of OL as a proxy of LS-II as determined by test weighing
the infant. They compared risk factor for delayed LS-II when using
MV vs. OL. MV was assessed by test weighing three times daily (0842 h
± 1:02, 1321 h ± 1:55 and 1846 h ± 1:02)
until women reported OL. Because continuous 24-h test weights were not
conducted, individual predictive curves were generated using a
second-order polynomial fit. Predicted MV was very accurate,
compared with empirical data. LS-II was considered delayed if the
predicted MV at 60 h postpartum was < 9.2 g/feed and OL was
defined as delayed if OL 
72 h postpartum. The
directionality and magnitude of the logistic regression coefficients
was remarkably consistent. Of the four risk factors identified for low
MV (first BF > 105 min postpartum, MV at 30 h postpartum,
and the interactions between obesity and breastfeeding frequency and
between parity and pumping), two were identified as significant (first
BF > 105 min postpartum, interaction between parity and pumping),
and the two remaining as marginally significant when OL was used as
outcome. The OL regression identified two risk factors as significant,
which were insignificant in the MV regression: emergency Cesarean
section and lower birth weight. Misclassification analysis conducted
with these data showed that OL has a good degree of specificity,
sensitivity, positive and negative predictive value, compared with MV
as a tool to identify individuals at risk of a delayed LS-II
(4
).
A number of studies that have included OL as the only marker of
lactogenesis have also consistently identified additional risk factors
for delayed OL. For example, studies in Indonesia (17
),
Mexico (18
), Honduras (19
) and the United
States (5
) have shown that conditions that limit infant
sucking, such as lack of rooming-in (17
, 18
),
prelacteal use (19
), or exclusive formula feeding
(5
), are associated with delayed OL. Likewise, three
independent studies from the United States (5
, 20
, 21
)
identified maternal obesity as a risk factor for delayed OL.
When does OL occur?
The overwhelming majority of women participating in prospective studies
have been able to report when they experienced OL
(3
, 5
, 12
, 16
, 21
). International studies have produced
estimates of mean OL time ranging from 50 to 73 h across studies
(4
–7
, 10
) and from 1 to 148 h within studies
(3
, 5
, 6
, 10
) (Hilson, J. and Rasmussen, K., personal
communication). The wide range for OL detected within samples is fully
consistent with the wide within sample LS-II variability as
determined by BMB or MV (1
–3
). Research studies conducted
in a variety of social and cultural settings suggest that 
25% of
women experience delayed OL (i.e., > 72 h after delivery)
(14
, 16
) (Hilson, J. and Rasmussen, K., personal
communication) and have identified risk factors for delayed OL
consistent with what is found when OL is expressed as a continuous
variable.
The initiation of LS-II as determined by BMB occurs between 24 and
48 h postpartum and plateaus at 60–84 h postpartum
(1
–3
). Likewise, MV data indicate that among U.S.
multiparous women, a significant increase in milk production starts at
36 h postpartum and levels off at 96 h postpartum
(11
).
What MV is transferred to the infant when women report OL?
Chapman et al. (15
) measured MV in a randomized trial in
Hartford, Connecticut designed to find out whether breast pumping
affects the timing of LS-II among women delivering by Cesarean
section. They compared the amount of milk consumed by the newborn
between women who perceive OL before 72 h (n = 26)
with those who perceived it 72 h (n = 18).
Subjects were included in the analyses only if they had a MV
measurement within 6 h after OL. The volume consumed at OL was
19.4 ± 12.3 mL and was similar among those perceiving OL < 72 h (18.7 ± 10.1 mL) vs. 72 h (20.4 ± 15.2
mL) (22
).
What cues do women use to identify OL?
Chapman and Pérez-Escamilla recently pooled data from two
prospective studies in Hartford, Connecticut (4
, 5
) to
identify the cues that women use to report OL, using factor analysis
(23
). All subjects were interviewed daily until OL was
reported. When subjects reported OL, they were then asked: "How did
you know that your milk came in?" OL symptoms reported by at least
4% of the sample were entered into the factor analysis, which
identified the following six components with an Eigen value > 1.0
explaining 62.8% of the total variance in symptoms: 1)
breast swelling, 2) milk leakage, 3) milk
physical appearance, 4) infant cues, 5) breast
fullness and 6) breast tingling.
Can women recall when OL occurred when interviewed months after delivery?
OL has also been assessed in retrospective studies (19
). A
longitudinal study from the United States (5
) was used to
compare actual and recalled timing of OL (24
). All 192
women were interviewed from d 1 postpartum until they reported OL,
which was corroborated against typical symptoms. Of the original
sample, 146 women were available for telephone follow-up at 6.7
± 1.5 mo postpartum. Misclassification analyses indicated that of
the 48 women who experienced delayed OL (i.e., > 72 h
postpartum), 45 were correctly identified at follow-up (i.e.,
Sensitivity = 93.8%). Fifty-one of the 81 women who
experienced an early OL were correctly identified with the recalled
data (Specificity = 63.0%).
What are the public health implications of delayed OL?
Retrospective (19
) and longitudinal studies
(4
, 18
, 25
) identified delayed OL as a risk factor for
shorter breastfeeding durations. In Hartford, Connecticut, two
independent studies found that this relationship occurred among women
who originally planned to breastfeed 6 mo but not among their
counterparts who were planning to breastfeed < 6 mo
(4
, 25
). It has been well established that early
introduction of infant formula (i.e., first days after delivery) is a
potent risk factor for the early termination of breastfeeding
(2
) even after controlling for original maternal
breastfeeding intentions (18
).
Dewey et al. (14
) found that whereas 35% of infants born
to women with an OL > 72 h postpartum had a weight loss
> 10% of birth weight by d 3 postpartum, this was the case only
for 6% of newborns whose mothers had an earlier OL.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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The wide range for OL detected within studies is fully consistent with the wide within sample LS-II variability as determined by BMB or infant breast milk consumption, indicating a high level of biological LS-II variability among individuals. As expected, OL is perceived when BMB and MV markers increase enough to be physically perceptible and perhaps when a minimum MV threshold is reached.
Mechanistic studies seeking to further understand the biological
determinants of the timing of LS-II should always use the most
accurate methods available. It is important, however, to recognize the
limitations from MV and BMB data. First, LS-II studies based on
infant test weighing actually measure infant breast milk intake and not
MV produced by the mammary gland. Second, although aggregate data may
allow for assessing the point at which the slope of the MV or BMB curve
starts to sharply increase, this is often not possible to determine for
individual subjects (3
, 4
). Third, we do not have a clear
definition of LS-II based on BMB. A variety of BMBs have been used
to assess LS-II, with the result being specific to the BMB
selected. Furthermore, the usefulness of the same BMB as a marker of
LS-II varies across studies [e.g., lactose (3
, 7
)].
Studies have used different approaches to define OL, including maternal
report of breast fullness (7
, 14
) and maternal report of
milk "coming in" (4
, 5
, 16
) (Hilson, J. and Rasmussen,
K., personal communication). In some studies, the assessment of OL is
not fully explained (3
, 6
, 9
, 10
, 12
, 13
). Furthermore, women
in different cultures use different term(s) to refer to the OL
phenomenon. Thus, multidisciplinary research is needed to further
refine the definition of OL and to standardize it across studies.
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FOOTNOTES |
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2 This is contribution # 2027 from the Storrs
Agricultural Experiment Station.
4 Abbreviations used: BMB, breast milk biomarker;
IDDM, insulin-dependent diabetes mellitus; LS-II, lactogenesis
stage II; MV, breast milk volume; OL, onset of lactation.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSCONCLUSIONSLITERATURE CITED |
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1. Neville, M. C., Morton, J. & Umemura, S. (2001) Lactogenesis: the transition from pregnancy to lactation. Pediatr. Clin. North Am. 48:35-52.[Medline]
2. Chapman, D. J. & Perez-Escamilla, R. (2000) Lactogenesis stage II: hormonal regulation, determinants and public health consequences. Recent Res. Dev. Nutr. 3:43-63.
3. Arthur, P. G., Smith, M. & Hartmann, P. E. (1989) Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. J. Pediatr. Gastroenterol. Nutr. 9:488-496.[Medline]
4. Chapman, D. J. & Perez-Escamilla, R. (2000) Maternal perception of the onset of lactation is a valid, public health indicator of lactogenesis stage II. J. Nutr. 130:2972-2980.
5. Chapman, D. J. & Perez-Escamilla, R. (1999) Identification of risk factors for delayed onset of lactation. J. Am. Diet. Assoc. 99:450-454.[Medline]
6. Hildebrandt, H. M. (1999) Maternal perception of lactogenesis time: a clinical report. J. Hum. Lact. 15:317-323.
7. Chen, D. C., Nommsen-Rivers, L., Dewey, K. G. & Lonnerdal, B. (1998) Stress during labor and delivery and early lactation performance. Am. J. Clin. Nutr. 68:335-344.[Abstract]
8. Neubauer, S. H., Ferris, A. M., Chase, C. G., Fanelli, J., Thompson, C. A., Lammi-Keefe, C. J., Clark, R. M., Jensen, R. G., Bendel, R. B. & Green, K. W. (1993) Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am. J. Clin. Nutr. 58:54-60.
9. Ferris, A. M., Neubauer, S. H., Bendel, R. B., Green, K. W., Ingardia, C. J. & Reece, E. A. (1993) Perinatal lactation protocol and outcome in mothers with and without insulin-dependent diabetes mellitus. Am. J. Clin. Nutr. 58:43-48.
10. Kulski, J. K., Smith, M. & Hartmann, P. E. (1981) Normal and caesarian section delivery and the initiation of lactation in women. Aust. J. Exp. Biol. Med. Sci. 59:405-412.[Medline]
11. Neville, M. C., Keller, R., Seacat, J., Lutes, V., Neifert, M., Casey, C., Allen, J. & Archer, P. (1988) Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am. J. Clin. Nutr. 48:1375-1386.
12. Vestermark, V., Hogdall, C. K., Birch, M., Plenov, G. & Toftager-Larsen, K. (1991) Influence of the mode of delivery on initiation of breast-feeding. Eur. J. Obstet. Gynecol. Reprod. Biol. 38:33-38.[Medline]
13. Schutzman, D. L., Hervada, A. R. & Branca, P. A. (1986) Effect of water supplementation of full-term newborns on arrival of milk in the nursing mother. Clin. Pediatr. 25:78-80.
14. Dewey, K. G., Nommsen-Rivers, L. A., Heinig, M. J. & Cohen, R. (2001) Lactogenesis and infant birth weight change in the first week of life. Davis, M. K. Isaacs, C. E. Hansen, L. A. Wright, A. eds. Integrating Population Outcomes, Biological Mechanisms, and Research Methods in the Study of Human milk and Lactation 2001 Kluwer Academic Plenum Publishers, New York, NY. (in press). .
15. Chapman, D. J., Young, S., Ferris, A. M. & Perez-Escamilla, R. (2001) Impact of breast pumping on lactogenesis stage II after cesarean delivery: a randomized clinical trial. Pediatrics (URL: http://www.pediatrics.org/cgi/content/full/107/6/e94) 107:E94.
16. Grajeda, R. (2001) The influence of stress during labor and delivery on the onset of lactation 2001 Department of Nutritional Sciences University of Connecticut, Storrs, CT. .
17. Mapata, S., Djauhariah, A. & Dasril, D. (1988) A study comparing rooming-in with separate nursing. Paediatr. Indones. 28:116-123.[Medline]
18. Pérez-Escamilla, R., Segura-Millan, S., Pollitt, E. & Dewey, K. G. (1993) Determinants of lactation performance across time in an urban population from Mexico. Soc. Sci. Med. 37:1069-1078.
19. Perez-Escamilla, R., Segura-Millan, S., Canahuati, J. & Allen, H. (1996) Prelacteal feeds are negatively associated with breast-feeding outcomes in Honduras. J. Nutr. 126:2765-2773.
20. Ferris, A. M., McCabe, L. T., Allen, L. H. & Pelto, G. H. (1987) Biological and sociocultural determinants of successful lactation among women in eastern Connecticut. J. Am. Diet. Assoc. 87:316-321.[Medline]
21. Rasmussen, K., Hilson, J. A. & Kjolhede, C. L. (2001) Obesity as a risk factor for failure to initiate and sustain lactation. Davis, M. K. Isaacs, C. E. Hanson, L. A. Wright, A. eds. Integrating Population Outcomes, Biological Mechanisms, and Research Methods in the Study of Human Milk and Lactation 2001 Kluwer Academic Plenum Publishers, New York, NY. (in press). .
22. Chapman, D. J. & Pérez-Escamilla, R. (2001) Milk transfer volume at the time of maternal perception of the onset of lactation. FASEB J 15:A1005.
23. Chapman, D. J. & Pérez-Escamilla, R. (2000) What cues do women use to identify the onset of lactation?. FASEB J 14:A508.
24. Pérez-Escamilla, R. & Chapman, D. (2001) Can women remember when their milk came in?. Newburg, D. eds. Bioactive Components of Human Milk 2001 Plenum Publishers New York, NY. pp 507–512. .
25. Chapman, D. J. & Pérez-Escamilla, R. (1999) Does delayed perception of the onset of lactation shorten breastfeeding duration?. J. Hum. Lact. 15:107-111.
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