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Detection of breastfeeding and weaning in modern human infants with carbon and nitrogen stable isotope ratios.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 129:279–293 (2006)
Detection of Breastfeeding and Weaning in Modern
Human Infants With Carbon and Nitrogen Stable
Isotope Ratios
B.T. Fuller,1,2* J.L. Fuller,3 D.A. Harris,2 and R.E.M. Hedges1
1
Research Laboratory for Archaeology and the History of Art, University of Oxford, Oxford OX1 3QJ,
United Kingdom
2
Department of Biochemistry, University of Oxford, Oxford OX1 3QU, United Kingdom
3
Sutter Auburn Faith Hospital, Auburn, California 95602
KEY WORDS
stable isotopes; paleodiet, fingernails; d13C; d15N
ABSTRACT
Carbon (13C/12C) and nitrogen (15N/14N)
stable isotope ratios were longitudinally measured in
fingernail and hair samples from mother-infant pairs
where infants were exclusively breastfed (n ¼ 5),
breast- and formula-fed (n ¼ 2), or exclusively formulafed (n ¼ 1) from birth. All exclusively breastfed infants
had a dual enrichment in carbon (1%) and nitrogen
(2–3%) when compared to maternal values. In contrast, breast- and formula-fed subjects had reduced
enrichments compared to exclusively breastfed subjects,
and the exclusively formula-fed infant showed no
increase in d13C or d15N values. This finding of a carbon trophic level effect in breastfeeding infants suggests
that 13C-enrichments of approximately 1% in archaeological populations are not necessarily the result of the
consumption of C4-based weaning foods such as maize
or millet. During the weaning process, the d13C results
for breastfed infants declined to maternal levels more
rapidly than the d15N results. This suggests that d13C
values have the potential to track the introduction of
solid foods into the diet, whereas d15N values monitor
the length of time of breast milk consumption. These
findings can be used to refine the isotopic analysis of
breastfeeding and weaning patterns in past and modern
populations. Am J Phys Anthropol 129:279–293, 2006.
Since the pioneering discovery that the nitrogen stable
isotope ratio (15N/14N) in body tissues can be used to
detect the age of weaning (Fogel et al., 1989), there have
been numerous applications of this technique to reconstruct breastfeeding and weaning patterns in archaeological populations (Katzenberg et al., 1993; Katzenberg and
Pfeiffer, 1995; Schurr, 1997, 1998; Herring et al., 1998;
Wright and Schwarcz, 1998, 1999; Dupras et al., 2001;
Mays et al., 2002; Richards et al., 2002; Schurr and
Powell, 2005). These studies of bone chemistry revealed
extensive information about the duration of breastfeeding
in different cultures and time periods, and give anthropologists a glimpse of societal views and health patterns that
are largely invisible in the archaeological record (Katzenberg et al., 1996). However, our understanding and interpretation of d15N values still rely on data from only two
controlled studies of three modern infants, even though
the use of nitrogen isotopic ratios in ancient infant nutrition has expanded and become routine (Fogel et al., 1989;
Millard, 2000). Thus, precise knowledge concerning the
magnitude of the isotopic fractionation and turnover time
of isotopic signatures during breastfeeding and weaning
in infants is limited. In addition, there has been only one
published study of how modern human infant d13C values
respond to the consumption of breast milk and weaning
foods, with this research reporting no change in d13C
results between a single breastfeeding mother-infant pair
(Fogel et al., 1989). However, subsequent studies of d13C
values from breastfed infants in archaeological populations suggested that individuals display a 1% increase in
d13C either as a result of breastfeeding or through the consumption of 13C-enriched C4 (the Hatch-Slack photosynthesis pathway)-based weaning foods such as maize and
millet (Katzenberg et al., 1993; Katzenberg and Pfeiffer,
1995; Wright and Schwarcz, 1999; Dupras et al., 2001;
Richards et al., 2002; Fuller et al., 2003). If d13C and d15N
signatures are to be effectively used to reconstruct breastfeeding and weaning patterns in archaeological and forensic material, then detailed longitudinal research on modern infants is necessary for comparison.
This study investigates the d13C and d15N signatures
in eight mother-infant pairs (Subjects A–H, mothers;
Subjects a–h, infants), where infants were exclusively
breastfed (n ¼ 5), breast- and formula-fed (n ¼ 2), or exclusively formula-fed (n ¼ 1) from birth. In order to conduct a
longitudinal study of the duration of breastfeeding and
the weaning period, we analyzed fingernail and hair samples taken at birth to a minimum age of 1 year from
mother-infant pairs residing in the town of Auburn, California. The proteins in sequential sections of fingernails
and hair provided a record of isotope ratios existing when
that material was synthesized (Fogel et al., 1989; O’Connell and Hedges, 1999). In addition, bovine milk-based (n
¼ 5) and soy-based (n ¼ 2) formulas were also analyzed for
d13C and d15N values to determine if unique isotopic signatures exist that could identify modern infants being fed
C 2005
V
WILEY-LISS, INC.
C
V
2005 Wiley-Liss, Inc.
*Correspondence to: Benjamin Fuller, P.O. Box 707, Auburn, CA
95604. E-mail: benjamin.fuller@sthughs-oxford.com
Received 4 May 2004; accepted 29 October 2004.
DOI 10.1002/ajpa.20249
Published online 31 October 2005 in Wiley InterScience
(www.interscience.wiley.com).
280
B.T. FULLER ET AL.
these different supplements. The findings of this research
have important implications regarding the isotopic interpretation of breastfeeding and weaning patterns in modern and past populations.
ISOTOPIC RECONSTRUCTION OF
BREASTFEEDING AND WEANING PATTERNS
The use of ratios from light stable isotopes (C, N, O, S,
and H) for both modern and ancient dietary reconstruction is predicated on the principle that ‘‘you are what you
eat’’ plus a small positive fractionation factor known as a
trophic level effect (DeNiro and Epstein, 1978; Kohn,
1999). Thus, the isotopic composition of the body will
reflect the isotopic signatures of foods and liquids consumed during life. In this case, the carbon and nitrogen
isotopic results of fingernails and hair will primarily
reflect the protein portion of the diet. For detailed reviews,
see Schwarcz and Schoeninger (1991), Schoeninger
(1995), and Kelly (2000). Stable isotope results are measured as the ratio of the heavier isotope to the lighter isotope (13C/12C or 15N/14N) and reported as d values in parts
per 1,000 or ‘‘per mil’’ (%) relative to internationally
defined standards for carbon (Vienna Pee Dee Belemnite,
vPDB) and nitrogen (ambient inhalable reservoir, AIR)
(Schwarcz and Schoeninger, 1991).
Since the groundbreaking experiments of Fogel et al.
(1989), d15N measurements have emerged as one of the
most successful techniques to elucidate breastfeeding and
weaning patterns in archaeological populations. Building
on previous research where each step up the food chain
was shown to increase d15N values by approximately 2–
4% (DeNiro and Epstein, 1981; Minagawa and Wada,
1984; Schoeninger and DeNiro, 1984), Fogel et al. (1989)
discovered that breastfeeding infants are also one trophic
level above their mothers in the food chain, since they are
essentially consuming their mother’s tissue through the
ingestion of breast milk. Thus, the d15N values of nursing
infants are elevated by 2–3% compared to the mother.
During the weaning process, the consumption of supplementary foods causes a decline in infant d15N values.
When a child is fully weaned (cessation of breastfeeding),
its protein d15N values are nearly identical to those of its
mother, assuming the mother-child pair has similar diets.
MATERIALS AND METHODS
Subjects
Eight mother-infant pairs (Subjects A–H, mothers; Subjects a–h, infants) participated in this study. All infants
were singleton births and were healthy during the period
of study. Written informed consent was obtained from the
mothers after a full explanation of the research. The protocol was approved by the Sutter Health Central Area
Institutional Review Committee (Sacramento, CA). The
mother of each subject recorded infant dietary habits,
including the timing of the introduction of solid foods
(duration and types of foods consumed) and the cessation
of breastfeeding.
Fingernail and hair analysis
Fingernails are an ideal medium to study dietary patterns in modern infants since they are metabolically inert,
resistant to degradation, isotopically representative of the
body protein pool, and have a fast synthesis rate. Fingernails were collected from subjects at various intervals dur-
ing the period of study. When sample size permitted, only
nail clippings from the three middle fingers were combined for analysis to reduce errors due to variations in
individual nail growth rates. Since fingernails grow out
from the cuticle but are collected at the fingertip, there is
a lag between sampling time and time of formation. For
infants, this lag is estimated to be 2–3 months, such that
the first sections analyzed were formed in utero (Fogel
et al., 1989), while the lag for adult fingernails is estimated to be slightly longer at 4–6 months (Runne and
Orfanos, 1981). For cleaning, fingernails were shotblasted to remove surface debris (dirt). Samples (1–1.5
mg) were then placed in tin capsules for isotopic analysis,
and combusted to CO2 and N2 in an automated carbon
and nitrogen analyzer (Carlo Erba, Milan, Italy) coupled
to a continuous-flow isotope-ratio-monitoring mass spectrometer (cf-irm-ms) (PDZ Europa Geo 20/20, Cheshire,
UK). When sample size permitted, all specimens were run
in triplicate, and analytical errors were typically less than
60.2% for d13C and d15N results.
For Subjects H and h, fingernail samples could not be
obtained, and hair was analyzed instead. The isotopic values recorded in hair are similar to those of fingernails
(O’Connell et al., 2001). Maternal hair samples (30–50
strands) were obtained at 8 weeks postpartum and were
measured in triplicate. Infant hair samples (20–40
strands) were obtained at three intervals: birth, age 10
weeks, and age 52 weeks. The hair from Subjects H and h
was then cut into 1-cm sections, corresponding to approximately 4 weeks of growth (Saitoh et al., 1969), and prepared for isotopic analysis following the protocol of O’Connell and Hedges (1999). Due to limited sample size, isotopic measurements were only performed once for Subject
h. Replicate measurement errors on known standards
within the run were less than 0.2% for d13C and 0.2% for
d15N.
Formula analysis
Infant formulas were collected from supermarkets in
Auburn, California and isotopically analyzed. The seven
different formulas were derived from either cow’s milk (n
¼ 5) or soybeans (n ¼ 2), with various supplements added
such as iron. As the ratio of carbon to nitrogen was high,
samples had to be analyzed separately for d13C (2–3 mg)
and d15N (10–12 mg) values. All samples were run in triplicate, and analytical errors were typically less than 60.2%
for d13C and d15N results.
RESULTS
Exclusively breastfed infants: Subjects a–e
The d13C and d15N results from mother-infant pairs
(Subjects A–E, mothers; Subjects a–e, infants) where the
infant was exclusively breastfed from birth are illustrated
in Figures 1–5 and listed in Table 1. Specific information
on the duration of breastfeeding and the timing and types
of solid foods consumed for these subjects is listed in
Table 2. During breastfeeding, Subjects a–e show a 13Cenrichment of approximately 1% above the mother’s fingernails. The infant d15N values are somewhat more variable, with approximate 15N-enrichments between 1.7–
2.8% compared to the mother’s fingernails. With the addition of solid foods to the diet, the infant d13C values
quickly decrease to levels below the maternal d13C values
(Figs. 1A, 2A, 3A, 4A, 5A). The infant d15N values also
decrease during the weaning process, but in comparison
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
281
Figs. 1A,B. Fingernail d13C (a) and d15N (b) results from Subject A (mother) and Subject a (infant) where Subject a was exclusively breastfed between 12–30 weeks. Specific dietary information for Subject a is listed in Table 2.
to the d13C results, the decline to maternal levels is generally slower and more gradual, with the exception of Subject e (Table 3). Subject e had the most abrupt weaning
period (14 weeks) and displayed a simultaneous drop in
carbon and nitrogen isotope ratios (Fig. 5A,B). At the cessation of breastfeeding, d13C values tend to increase
slightly and then display no general pattern. The d15N
results stabilize and change little after the cessation of
breastfeeding.
Breast- and formula-fed infants: Subjects f–g
The results from the two infants who were breast- and
formula-fed from birth are presented in Figures 6 and 7
282
B.T. FULLER ET AL.
Figs. 2A,B. Fingernail d13C (a) and d15N (b) results from Subject B (mother) and Subject b (infant) where Subject b was exclusively breastfed between 12–32 weeks. Specific dietary information for Subject b is listed in Table 2.
and listed in Table 1. Subject f was breast- and formulafed with Similac1 with iron (180 ml/day) from birth, and
displays a small increase in d13C (0.5%) and d15N
(1.0%) values during the period of breast- and bottlefeeding (Fig. 6). The start of solid food consumption (rice
cereal, chicken, lamb, potatoes, pineapple, and spaghetti)
at 30 weeks causes d13C and d15N results to decrease to
maternal values. Between 35–45 weeks, Subject f began
eating all of the adult table foods in addition to breastand formula-feeding. Subject f was still breastfeeding
(mainly for comfort) at time of last sampling at 51 weeks,
and the d15N values remained elevated at this point, while
the d13C results were below those of Subject F (Fig. 6).
Subject g was breast- and formula-fed with Isomil1 soy
(30–60 ml/day) from birth and displayed an increase in
d13C (0.5%) and d15N (1.4%) during this period (Fig.
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
283
Figs. 3A,B. Fingernail d13C (a) and d15N (b) results from Subject C (mother) and Subject c (infant) where Subject c was exclusively breastfed between 14–47 weeks. Specific dietary information for Subject c is listed in Table 2.
7). At 25 weeks, Subject g was changed to exclusive nursing for a period of 9 weeks. During this time of exclusive
breastfeeding, 13C-enrichment (1%) and 15N-enrichment
(3%) were observed. Solid foods (oatmeal, green beans,
apples, and pears) were introduced to the diet at week 34,
and this resulted in a decrease in d13C and d15N values. Cessation of breastfeeding occurred during week 58, and the
subject was eating all of the adult table foods by week 60.
Exclusively formula-fed infant: Subject h
The results from the only exclusively formula-fed infant
are illustrated in Figure 8 and listed in Table 1. Since fingernails were not obtained from Subject h, hair was analyzed. During the bottle-feeding period (350 ml/day of
Carnation Good Start1), there was no increase in d13C or
d15N results, but rather a decrease of 0.5% for carbon
284
B.T. FULLER ET AL.
Figs. 4A,B. Fingernail d13C (a) and d15N (b) results from Subject D (mother) and Subject d (infant) where Subject d was exclusively breastfed between 12–32 weeks. Specific dietary information for Subject d is listed in Table 2.
and 2.0% for nitrogen. Solid foods were first introduced
to the diet at week 22 (rice cereal, bananas, peaches, apricots, and plums), and at week 26, vegetables (sweet potatoes, potatoes, green beans, corn, and squash) were introduced. The addition of fruits and vegetables to the diet
caused d13C and d15N values to recover to those seen at
birth. Subject h began consuming meat (chicken and turkey) and dairy products (milk) at week 35, and by week 44
all adult table foods were part of the diet. At time of last
sampling, d13C and d15N values were relatively stable at
17.9% and 8.9%, respectively, and Subject h was still
consuming formula in addition to table foods.
Formula
The results from the seven formulas analyzed for d13C
and d15N values are presented in Table 4. The formulas
were synthesized from either cow’s milk (n ¼ 5) or soybeans (n ¼ 2), and represent four different commercial
brands found in Northern California. The majority of
milk-based supplements had d13C values between 21.9%
and 23.2%, and d15N values between 4–5%. However,
the Enfamil1 milk-based formula had significantly
enriched d13C (19.9%) and d15N (7.5%) results. Both of
the soy-based formulas had d13C values that were similar
to those derived from cow’s milk, but the d15N values were
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
285
Figs. 5A,B. Fingernail d13C (a) and d15N (b) results from Subject E (mother) and Subject e (infant) where Subject e was exclusively breastfed between 12–19 weeks. In contrast to Subjects a–d, Subject e displays a simultaneous decrease in d13C and d15N values during the weaning period. Specific dietary information for Subject e is listed in Table 2.
significantly lower at 0.5%. Since d15N values increase in
tandem with each step up the food chain, this difference
between soy- and cow milk-based formulas can be attributed to this food chain phenomenon.
DISCUSSION
Pregnancy and possible in utero effects in
mother-infant pairs
The mothers’ fingernail and hair d13C results (Subjects
A–H) do not show a systematic variation during preg-
nancy and lactation. In contrast, during the first 12–14
weeks (fingernails formed in utero), 7 of 8 infants (except
Subject f) have fetal d13C values that decrease toward
time of birth (Figs. 1A, 2A, 3A, 4A, 5A, 6A, 7A, 8A). We
speculate that this decline in d13C could be the result of a
small change (0.5%) in carbon metabolism in either the
mother or fetus, or a variation in the placental uptake
and/or transport of carbon. Further research is necessary
to fully understand this observation.
All mothers (except Subject B) have d15N results that
decrease by approximately 0.5–1% between 10 to 20
weeks of infant age (Figs. 1B, 2B, 3B, 4B, 5B, 6B, 7B, 8B).
286
B.T. FULLER ET AL.
TABLE 1. C and N results for mother-infant pairs1
13
Subject
A
a
B
b
C
15
TABLE 1. (Continued)
Sampling
time (weeks)
d13C (%)
6SD
d15N (%)
6SD
Subject
25
12
6
3
7
12
15
27
36
43
54
0
6
12
14
22
27
29
33
37
45
59
63
67
0
4
8
14
21
28
33
40
44
47
52
57
66
72
77
80
1
8
9
13
16
19
22
25
30
34
39
43
48
52
57
61
66
70
74
79
10
2
5
14
23
34
54
81
18.1
17.9
17.8
18.0
17.8
18.0
18.2
18.3
17.7
17.8
18.2
17.4
17.5
17.6
17.1
16.5
16.7
17.1
18.0
18.9
19.0
18.5
17.7
18.1
18.1
18.0
18.1
18.1
17.7
17.6
17.7
17.7
17.7
17.6
17.8
17.6
18.0
17.7
17.7
17.8
17.5
17.7
17.8
17.2
17.1
17.1
17.2
17.2
17.4
17.4
17.9
18.3
18.8
18.7
18.1
18.1
18.6
18.6
18.5
19.0
18.2
18.4
18.6
18.2
18.4
18.6
18.2
18.4
0.1
0.2
0.2
0.1
0.2
0.1
0.1
0.2
0.1
0.2
0.1
nd
nd
0.1
0.1
0.1
0.2
nd
nd
0.1
0.2
0.4
0.2
0.2
0.2
0.1
0.1
0.1
<0.05
0.2
0.1
0.1
0.1
0.2
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.2
0.2
0.1
nd
0.1
0.1
0.1
0.1
0.1
0.3
0.2
0.2
0.1
0.1
0.1
0.1
0.2
0.2
0.1
0.2
0.1
0.1
0.1
0.1
nd
0.1
9.3
9.2
9.4
9.4
9.0
8.7
8.8
9.1
9.3
8.9
8.7
8.5
8.6
8.7
9.7
11.4
11.8
11.9
11.3
10.6
10.0
10.3
9.6
9.6
9.2
9.2
9.2
9.1
9.4
9.0
9.0
8.9
9.0
8.9
8.8
9.2
9.1
9.2
9.3
9.3
9.4
9.3
9.6
10.2
10.4
10.6
10.6
11.2
11.2
11.3
11.3
10.6
9.1
8.7
8.5
8.4
9.1
8.7
8.8
8.7
9.2
9.0
8.8
9.0
9.2
8.9
8.9
9.0
0.1
<0.05
0.1
<0.05
0.2
0.1
0.1
0.2
0.2
<0.05
0.3
nd
nd
0.2
0.2
0.1
0.1
nd
nd
0.3
0.2
0.1
0.2
0.3
<0.05
0.1
<0.05
<0.05
0.1
0.1
0.1
0.1
0.1
0.2
0.1
0.2
<0.05
0.1
0.1
0.1
0.2
0.2
0.1
0.4
0.3
nd
0.2
0.2
0.1
0.2
0.1
0.3
0.1
0.1
0.3
0.2
0.2
0.1
0.1
0.1
0.1
0.1
0.2
0.2
0.2
0.1
nd
0.1
c
D
d
E
e
Sampling
time (weeks)
d13C (%)
6SD
d15N (%)
6SD
2
7
9
11
14
18
22
25
31
34
40
50
55
81
4
0
7
17
27
37
45
54
61
76
80
0
8
17
28
38
41
44
48
52
55
61
66
78
85
14
7
3
1
10
14
20
24
31
33
61
65
71
1
8
10
13
15
20
23
25
29
32
37
41
47
51
62
66
18.1
18.6
18.2
18.5
18.5
17.6
17.8
17.9
17.8
17.8
17.7
17.5
18.0
18.2
18.8
19.0
19.2
18.4
18.4
18.4
18.4
18.5
18.1
18.1
18.0
18.5
19.0
17.6
17.9
18.2
18.9
18.9
19.5
19.5
19.4
19.1
19.0
19.1
18.5
18.5
18.0
17.8
18.0
18.1
17.7
17.7
17.8
18.0
18.2
17.7
18.0
17.6
17.5
17.6
17.5
17.0
16.6
16.7
17.1
17.3
18.4
18.5
18.2
18.0
17.8
18.0
18.8
19.1
0.3
0.1
0.2
0.1
0.2
0.2
0.1
0.1
0.1
0.1
0.1
0.1
0.2
0.2
0.1
0.1
0.1
0.1
0.2
0.2
0.2
0.3
0.1
0.3
0.1
nd
nd
nd
0.2
0.2
0.3
0.3
0.1
0.1
0.3
0.1
0.1
0.1
0.1
0.2
nd
0.1
0.1
0.2
0.1
0.2
0.3
0.2
0.2
<0.05
0.1
<0.05
nd
0.1
0.2
0.2
0.2
0.1
<0.05
0.2
0.4
0.1
0.1
0.1
0.1
0.1
0.3
0.1
9.8
9.8
10.0
9.8
9.4
11.0
10.9
10.6
11.0
11.1
11.5
11.7
11.4
10.4
9.0
8.4
8.1
8.2
8.0
7.6
7.6
8.0
8.1
8.4
8.6
8.4
8.7
10.3
10.9
10.9
10.4
10.1
9.8
9.7
9.5
9.1
9.0
9.3
9.3
9.6
9.2
9.2
9.0
8.7
8.8
9.1
9.3
9.3
9.3
9.1
9.3
9.3
9.5
9.4
9.5
9.8
10.9
10.8
10.4
9.9
8.1
8.1
9.0
9.0
9.1
9.1
9.4
9.6
0.1
0.2
0.3
0.3
0.1
0.2
0.1
0.2
0.2
0.1
0.2
0.4
0.1
0.2
0.3
0.1
0.1
0.1
0.1
0.1
0.2
0.4
0.2
0.2
0.1
nd
nd
nd
0.3
0.2
0.2
0.1
<0.05
<0.05
0.3
0.3
0.2
0.2
0.1
0.3
nd
0.3
0.2
0.2
0.1
0.1
0.2
0.1
<0.05
0.2
0.2
<0.05
nd
0.2
0.1
0.3
0.1
0.1
0.1
0.3
0.3
0.2
0.3
<0.05
0.3
0.4
0.1
0.2
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
TABLE 1. (Continued)
Subject
F
f
G
g
H
h
Sampling
time (weeks)
d13C (%)
6SD
d15N (%)
6SD
18
14
4
0
3
10
15
18
26
34
48
3
10
14
15
19
24
27
32
34
48
51
22
8
3
3
17
22
44
52
2
7
16
22
26
29
32
38
48
77
20
16
12
8
4
0
4
8
4
0
6
10
20
24
28
32
36
40
44
48
52
19.2
19.0
18.3
18.7
18.5
18.8
18.9
18.5
18.9
18.7
18.7
19.0
18.9
18.2
18.2
18.5
18.4
18.5
18.8
18.9
19.4
19.1
18.2
17.7
17.8
17.6
18.3
18.0
17.2
17.3
17.8
18.1
17.1
17.4
17.2
16.9
17.1
17.6
18.4
18.3
17.1
17.0
16.8
16.8
17.1
16.8
17.3
16.9
16.4
17.1
16.5
16.7
17.3
16.9
16.5
16.5
17.1
17.7
18.0
17.9
17.9
0.1
0.3
0.1
0.2
<0.05
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.2
0.2
0.1
<0.05
0.1
0.2
0.1
0.3
0.1
0.2
0.1
0.1
0.1
0.2
0.1
0.3
nd
0.1
nd
0.1
0.1
0.1
0.1
0.2
0.1
0.4
<0.05
0.1
<0.05
<0.05
<0.05
<0.05
0.2
0.3
0.3
<0.05
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
9.5
9.6
8.9
8.9
9.1
9.4
9.7
9.8
9.7
9.6
9.4
10.0
10.0
10.5
10.3
10.0
10.7
11.0
10.6
10.9
10.1
10.5
9.4
9.8
9.6
9.4
8.8
9.6
9.5
9.7
9.9
9.9
10.7
11.3
11.8
12.2
12.4
11.8
10.4
9.2
9.1
9.2
9.1
8.9
8.7
8.5
8.9
9.4
9.4
9.0
9.0
9.3
7.2
8.1
8.6
9.2
9.0
9.0
8.8
9.0
8.9
0.1
0.3
0.2
0.1
0.2
<0.05
<0.05
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.3
0.2
0.4
0.1
0.4
<0.05
0.1
<0.05
<0.05
0.1
0.2
nd
0.1
nd
<0.05
0.1
0.1
0.1
0.1
0.1
0.4
0.3
<0.05
0.1
0.1
<0.05
<0.05
0.1
0.2
<0.05
0.1
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
1
Subjects A–H, mothers; Subjects a–h, infants. Measurements were
made in triplicate except where indicated (nd). A sampling time of
0 ¼ birth; negative week values are sampling times before birth.
This decline in maternal d15N values can be attributed to
the pregnancy effect, and is likely the result of the maternal conservation of nitrogen for the growing fetus during
287
gestation (Fuller et al., 2004). Two subjects (c and h; Figs.
3B, 8B) have in utero d15N results that seem to track the
decrease in maternal values, and Millard (2000) noted
that the three infants in his study all had lower fetal d15N
values than predicted. These findings suggest the possibility that fetal d15N values parallel the decline in maternal
d15N results during pregnancy. However, more specific
research is needed to discover if there is a link between
the falling d13C and d15N values and maternal metabolism, and to understand why some subjects show evidence
of a decrease in fetal d15N values, while others do not.
Breastfeeding, weaning, and infant d15N values
The fingernails of exclusively breastfed subjects display
the expected d15N increase during breastfeeding, but
there is a wide range in 15N-enrichments (1.7–2.8%). This
greater variability can be attributed to the fact that in
addition to diet, d15N values are influenced by the nitrogen balance of an individual. Positive nitrogen balance
(growth) was shown to decrease d15N values, and negative
nitrogen balance (nutritional stress) results in increased
d15N values (Hobson and Clark, 1992; Hobson et al.,
1993; Gannes et al., 1997; Fuller et al., 2004). Additional
research is necessary to better understand the relationships among infant weight gain, diet (maternal breast
milk protein content), and 15N-enrichment during breastfeeding. During the weaning process, all of the infant
d15N values decline toward the maternal values, and this
reflects the consumption of foods with lower d15N values
than breast milk protein (d15N ¼ 8–9%, Fuller, 2003). This
decrease in d15N during weaning was slower compared to
the d13C results, and this will be discussed in detail below
(Table 3).
The d15N values of the two breast- and formula-fed subjects (f and g) are also 15N-enriched by approximately
1.0% and 1.4%, respectively. This reduced 15N-enrichment shows that the infant tissue nitrogen is being
derived from both the breast milk protein (d15N ¼ 8–9%;
Fuller, 2003) and the bovine milk formula (d15N ¼ 4–5%).
It is significant to note that after being breast- and bottlefed from birth, Subject g switched to a period of exclusive
breastfeeding between 25–34 weeks (Fig. 7b). During this
interval, the d15N ( 3%) results increased to levels seen
in infants who were exclusively breastfed from birth.
Thus, as seen in a previous study of horse hair (West
et al., 2004), the infant fingernail data here also support
the finding that consumer protein is very quick to register
the isotopic signals of a dietary change.
The only exclusively formula-fed infant (Subject h)
shows no increase in d15N, and actually decreases by
approximately 2.0% (Fig. 8B). This decrease in d15N during exclusive formula-feeding confirms that the 15Nenrichment observed during exclusive breastfeeding is the
result of the trophic level effect (Fogel et al., 1989). The
formula (Carnation Good Start1) consumed by Subject h
had a d15N value of 4.3% (Table 4). Thus, the d15N value
of 7.2% at 20 weeks is 2.9% enriched above the formula
(Fig. 8b), and this is near the high end of 15N-enrichments
(1.7–2.8%) for exclusively breastfed Subjects a–e. Since
infant formula is usually higher in protein content compared to breast milk, it is hypothesized that bottle-fed
infants may have higher diet-to-tissue-trophic-level fractionation factors compared to breastfed infants. More
research is necessary to explore this possibility.
288
B.T. FULLER ET AL.
TABLE 2. Timing of weaning process and the foods consumed by exclusively breastfed Subjects a–e
Subject
Period of exclusive
breastfeeding1
a
12–30 weeks
b
12–32 weeks
c
14–47 weeks
d
12–32 weeks
e
12–19 weeks
Timing of weaning process
and foods consumed
Cessation of
breastfeeding
Weaning week 30: Rice cereal started
once a day.
Week 35: Peas and bananas started
once a day.
Week 48: Rice cereal, bananas, peas,
applesauce, and sweet potatoes.
Week 57: Oatmeal, peas, bananas,
spaghetti, applesauce, chicken pasta,
and 440 ml of Carnation Good Start1 a day.
Week 66: All adult table foods eaten and
440 ml/day of Carnation Good Start1.
Weaning week 32: Rice cereal started
once a day.
Week 42: Rice, oat, and barley cereal,
green beans, and corn tortillas.
Week 44: Started 120–240 ml/day of
Enfamil1 with iron.
Week 52: Rice and oat cereal, applesauce, chicken,
peas, carrots, sweet potatoes, peaches, pears,
bananas, and 120–240 ml/day of Enfamil1 with iron.
Week 60: All adult table foods eaten plus
120–240 ml/day of Enfamil1 with iron.
Week 64: All adult table foods eaten plus
300 ml/day of Enfamil1 with iron, and
300 ml/day of lowfat cow’s milk.
Week 76: All adult table foods eaten.
Weaning week 47: 1 cup of rice or wheat
cereal in breast milk started once a day,
carrots, and squash.
Week 60: 1 cup of rice or wheat cereal in
breast milk, carrots, squash, apples, pears,
crackers, grape juice, and apple juice.
Week 68: Rice or oat cereal, cheese, crackers,
yogurt, apples, pasta, tomatoes, chicken, rice, corn
chips, and bagels.
Week 78: All adult table foods eaten.
Weaning week 32: Rice cereal, oatmeal, apples,
bananas, peaches, apricots, and blueberries.
Week 46: Turkey and egg yolk started.
Week 50: Cottage cheese, tofu, sweet potatoes,
green beans, broccoli, cauliflower, and yogurt.
Week 60: All adult table foods eaten.
Weaning week 19: Started 120 ml/day of
Similac1 with iron.
Week 30: Rice cereal started once a day.
Week 40: Rice cereal, carrots, peas, apples, bananas,
and formula-feeding with Similac1 with iron.
Week 66
Week 56
Subject still breastfeeding
at every meal at time
of last sampling.
Week 67
Week 33
1
There is a time lag between period of fingernail growth and sampling. Real-time isotopic signatures can be obtained by subtracting 12 weeks (Subjects a, b, d, e) or 14 weeks (Subject c) from times listed.
Breastfeeding, weaning, and infant d13C values
The findings of this study clearly demonstrate an intrinsic 13C-enrichment of 1% in the fingernail proteins of
exclusively breastfed human infants. The breast- and formula-fed subjects also displayed 13C-enrichments of
approximately 0.5%, while the exclusively bottle-fed individual showed no increase in d13C values (Fig. 8A). This
discovery of a carbon trophic-level shift in modern breastfeeding infants is in contrast to the results of Fogel et al.
(1989), and suggests that 13C-enrichments of approximately 1% in archaeological populations are not necessarily indicative of the consumption of C4-based weaning
foods such as maize or millet. During the weaning process,
the d13C results for breastfed infants declined to maternal
levels more rapidly than the d15N results (Table 3). This
faster return of infant d13C values to maternal d13C values
was seen in all subjects except Subject e. Subject e was
weaned the most abruptly and displayed a nearly simultaneous decrease in both d13C and d15N values (Fig. 5A,B).
The cause of this faster decline in d13C values during
weaning is not fully understood, but we speculate that it
could be the result of a combination of two possible mechanisms. First, infants’ 13C-enrichment over the mothers’
fingernails is only 1% compared to 2–3% for 15N-enrichment. Thus, this greater increase in infant d15N values
during breastfeeding also means that it will take longer
for d15N values to return to maternal levels during weaning. Second, since the weaning foods (rice cereal, oatmeal,
fruits, and vegetables) that these subjects consumed are
more rich in carbohydrates than protein, the dilution in
the infant carbon pool will be greater when compared to
289
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
TABLE 3. Time when breastfeeding infant C and N values
return to maternal levels during the weaning period1
13
15
Subject
Time when infant
d13C values return to
maternal d13C levels
Time when infant
d15N values return to
maternal d15N levels
a
33 weeks
b
c
37 weeks
81 weeks
d
39 weeks
e
f
27 weeks
32 weeks
g
h
38 weeks
NA
Still elevated (0.5%)
at 67 weeks
50 weeks
Still elevated (1.4%)
at 81 weeks
Still elevated (0.9%)
at 85 weeks
27 weeks
Still elevated (1.1%)
at 51 weeks
50 weeks
NA
1
For d15N results, some subjects are still elevated at time of
last sampling. Subject h was formula-fed from birth, so no
results could be obtained (NA).
the nitrogen pool, which is still being primarily derived
from the high-quality protein in breast milk. While no isotopic measurements were made on the weaning foods,
d13C results from a previous study (Schoeller et al., 1986)
of cereals, fruits, and vegetables from Chicago, Illinois,
showed that these foods (which are similar to the weaning
foods) are 13C-depleted (23% to 29%) compared to the
breast milk protein (19.5%) and whole breast milk
(22% to 23%) that these infants were consuming
(Fuller, 2003). Thus, this faster decrease in d13C could be
the result of the more pronounced dilution of breast milk
carbon with the 13C-depleted carbon content in the weaning foods. It is hoped that advances in the isotopic measurement of carbon and nitrogen single amino acids (Fogel
and Tuross, 2003; Corr et al., 2005; McClelland and Montoya, 2002; Schmidt et al., 2004) and carbohydrates will
permit a more detailed investigation of this topic by tracing how breast milk and weaning foods are incorporated
into infant protein.
The findings that d13C values are elevated by approximately 1% during exclusive breastfeeding and that d13C
values return more quickly than d15N values to maternal
levels during weaning have important ramifications for
the interpretation of breastfeeding and weaning patterns
in archaeological populations. Currently, the most accepted
method for determining the age of weaning is by measuring
d15N values in bone collagen from different age classes
of infants and children, and noting the age at which d15N
values return to those of the adult female population
(Katzenberg et al., 1993; Schurr, 1997; Dupras et al.,
2001; Mays et al., 2002; Schurr and Powell, 2005). Little
significance has been attributed to bone collagen d13C
values, as they rarely display unique isotopic patterns
similar to those of d15N results, although a number of stud-
13
ies noted C-enrichments (0.5–1.4%) and attributed these
to either a possible tropic-level effect of breastfeeding or
the consumption of C4-based foods (maize or millet)
(Katzenberg et al., 1993; Katzenberg and Pfeiffer, 1995;
Wright and Schwarcz, 1999; Dupras et al., 2001; Richards
et al., 2002). In addition, research from dentine serial sections from the Medieval site of Wharram Percy, where no
C4 dietary items were present, identified a 13C-enrichment
(1%) that was likely the result of breastfeeding (Fuller
et al., 2003).
Based on the d13C results from this current study, we
suggest that infant bone collagen d13C values might yield
information that is as important as d15N values in determining ancient breastfeeding and weaning patterns. In
particular, the fact that d13C values return faster than
d15N values to maternal levels suggests that d13C values
can be used as a possible indicator for the introduction of
solid foods to the diet, whereas d15N values seem to be better suited to monitor the duration of breast milk consumption or the nitrogen trophic-level effect of breastfeeding.
Subject a (Fig. 1A,B) provides a perfect example for this
argument. For Subject a, the point at 33 weeks is higher
than the mean maternal d15N value by 2.2% but equal to
the mean maternal d13C value. If the d13C and d15N values
for Subject a at point 33 were bone collagen results, the
elevated d15N value would be interpreted as evidence of
exclusive breastfeeding, but there would be no mention of
d13C value, since it is equal to the mean maternal d13C
value. However, using the present study as a model, it
would be possible to correctly identify this individual as
eating solid foods while still breastfeeding.
The fact that many archaeological studies on weaning
found elevated d15N values without increased d13C values
suggests the possibility that the infants were dying while
still breastfeeding but were also in the process of consuming solid foods. From a medical point of view, this observation is not surprising or unfounded, since the introduction
of solid foods to the infant diet is clearly linked to an
increased risk of infant mortality because of the exposure
to new pathogens, nutritional stress, and a decrease in
immunity levels (Knodel and Kintner, 1977; Katzenberg
et al., 1996; Lönnerdal, 2000). However, given the modest
sample size of this study, caution should be applied when
using these results as the only models for archaeological
interpretation. More isotopic research is needed on modern infants from outside North America (from countries
where there is less consumption of C4 foods) to confirm if
d13C values can be used as a unique marker for the introduction of solid foods during weaning. In addition, it would
be interesting to examine how the consumption of 13Cenriched C4-derived weaning foods (such as maize and millet) affects the isotopic results of modern infants. In conclusion, the combined analysis of infant d13C and d15N values has the potential to become an enhanced technique for
examining both the timing of the weaning process and the
cessation of breastfeeding in modern and past populations.
TABLE 4. 13C and 15N results from bovine milk-based and soy-based infant formulas from Northern California
Formula
d13C (%)
6SD
d15N (%)
6SD
Enfamil (soy-based)
Enfamil1 (milk-based)
Enfamil1 (milk-based with iron)
Similac1 (milk-based with iron)
Similac1 (milk-based low iron)
Isomil1 (soy-based)
Carnation Good Start1 (milk-based)
19.8
19.9
23.1
23.2
22.7
21.7
21.9
0.2
0.1
0.1
0.1
0.1
0.1
0.1
0.5
7.5
4.5
4.9
4.7
0.2
4.3
0.3
0.4
0.3
0.2
0.3
0.4
0.1
1
290
B.T. FULLER ET AL.
Figs. 6A,B. Fingernail d13C (a) and d15N (b) results from Subject F (mother) and Subject f (infant) where Subject f was breastand formula-fed between 12–30 weeks. Compared to the exclusively breastfed infants (Subjects a–e), Subject f displayed reduced
13
C- and 15N-enrichments. Specific dietary information for Subject f is discussed in Results.
Formula
The d13C and d15N results from infant formulas show
that there are isotopic distinctions between the soy- and
cow milk-based products (Table 4). While the number of
formulas studied was small (n ¼ 7), modern infants who
consume soy-based formulas should display tissue d15N
values that are lower compared to individuals fed bovine
milk-based supplements, and this could potentially distinguish among subjects fed these different formulas. However, more isotopic research is necessary on infant formulas from different locations to determine the extent of
differences in isotopic signatures between soy- and milkbased formulas.
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
291
Figs. 7A,B. Fingernail d13C (a) and d15N (b) results from Subject G (mother) and Subject g (infant) where Subject g was breast- and
formula-fed between 12–25 weeks. Between 25–34 weeks, Subject g was exclusive breastfed and displays increased 13C- (1%) and
15
N-enrichments (3%) compared to the breast- and formula-fed period. Specific dietary information for Subject g is discussed in
Results.
CONCLUSIONS
We conducted a longitudinal study of d13C and d15N
signatures in eight mother-infant pairs where infants
were exclusively breastfed, breast- and formula-fed, or
exclusively formula-fed from birth. All exclusively
breastfed subjects displayed enrichments in 13C (1%)
and 15N (2–3%) compared to maternal values. Individuals who were fed both breast milk and formula
showed reduced enrichments in 13C and 15N, but the
infant who exclusively consumed formula from birth
displayed no trophic-level enrichments in carbon or
nitrogen compared to maternal values. These findings
demonstrate a dual increase in d13C and d15N values of
tissue proteins during nursing, and show that 13Cenrichments of 1% in archaeological populations are
not necessarily the result of a weaning diet based on
maize or millet.
292
B.T. FULLER ET AL.
Figs. 8A,B. Hair d13C (a) and d15N (b) results from Subject H (mother) and Subject h (infant) where Subject h was exclusively formula-fed between 0–22 weeks and does not show elevated d13C and d15N values compared to maternal levels. Specific dietary information for Subject h is discussed in Results.
During the weaning process, the d13C results for
breastfed infants declined to maternal levels more rapidly than the d15N results. Thus, based on the results
of this small study, d13C values seem to be more sensitive to the introduction of solid foods to the diet,
whereas d15N values appear to monitor the duration of
breast milk consumption by an infant or the trophiclevel effect of breastfeeding. While more research is
needed from breastfed infants fed isotopically different
diets, it is likely that the combined analysis of d13C
and d15N values will refine the interpretation of infant
nutrition in past populations. In addition, this technique is simple, inexpensive, and noninvasive, and can
be used in medical and forensic research to detect
breastfeeding and weaning patterns in modern human
populations.
ISOTOPIC SIGNATURES OF BREASTFEEDING AND WEANING
ACKNOWLEDGMENTS
We are greatly indebted to all parents and subjects who
participated in this study. Without their help, interest,
and enthusiasm, this research would not have been possible. We gratefully acknowledge the help of Nancy Sage,
and all the nurses of the OB/GYN Department at Sutter
Auburn Faith Hospital in the collection of dietary histories and samples. Thanks go to Peter Ditchfield, Martin
Humm, Angela Bowles, and Christine Tompkins for
technical assistance and advice during isotopic analysis.
This manuscript was greatly improved by the comments
and suggestions of Mandy Jay, Vaughan Grimes, and
three anonymous reviewers.
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