Content uploaded by Kathryn Coe
Author content
All content in this area was uploaded by Kathryn Coe
Content may be subject to copyright.
This article was downloaded by: [The University of Texas at El Paso]
On: 14 February 2013, At: 11:56
Publisher: Routledge
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered
office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Ecology of Food and Nutrition
Publication details, including instructions for authors and
subscription information:
http://www.tandfonline.com/loi/gefn20
Food Aversions and Cravings during Early
Pregnancy: Association with Nausea and
Vomiting
M. Margaret Weigel a , Kathryn Coe b , Nancy P. Castro c , Maria
Elena Caiza d , Nora Tello e & Monica Reyes c
a Human Nutrition and Immunology Research Laboratory,
Department of Public Health Sciences, College of Health Sciences,
University of Texas at El Paso, El Paso, Texas, USA
b Department of Public Health, School of Medicine, Indiana
University, Indianapolis, Indiana, USA
c College of Agriculture, Foods, and Nutrition, Universidad San
Francisco de Quito, Quito, Ecuador
d Ministerio de Salud Publica, Quito, Ecuador
e Hospital Baca Ortiz, Quito, Ecuador
Version of record first published: 29 Apr 2011.
To cite this article: M. Margaret Weigel , Kathryn Coe , Nancy P. Castro , Maria Elena Caiza , Nora
Tello & Monica Reyes (2011): Food Aversions and Cravings during Early Pregnancy: Association with
Nausea and Vomiting, Ecology of Food and Nutrition, 50:3, 197-214
To link to this article: http://dx.doi.org/10.1080/03670244.2011.568906
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Any
substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,
systematic supply, or distribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation
that the contents will be complete or accurate or up to date. The accuracy of any
instructions, formulae, and drug doses should be independently verified with primary
sources. The publisher shall not be liable for any loss, actions, claims, proceedings,
demand, or costs or damages whatsoever or howsoever caused arising directly or
indirectly in connection with or arising out of the use of this material.
Ecology of Food and Nutrition, 50:197–214, 2011
Copyright ©Taylor & Francis Group, LLC
ISSN: 0367-0244 print/1543-5237 online
DOI: 10.1080/03670244.2011.568906
Food Aversions and Cravings during Early
Pregnancy: Association with Nausea
and Vomiting
M. MARGARET WEIGEL
Human Nutrition and Immunology Research Laboratory, Department of Public
Health Sciences, College of Health Sciences, University of Texas at El Paso,
El Paso, Texas, USA
KATHRYN COE
Department of Public Health, School of Medicine, Indiana University,
Indianapolis, Indiana, USA
NANCY P. CASTRO
College of Agriculture, Foods, and Nutrition, Universidad San Francisco
de Quito, Quito, Ecuador
MARIA ELENA CAIZA
Ministerio de Salud Publica, Quito, Ecuador
NORA TELLO
Hospital Baca Ortiz, Quito, Ecuador
MONICA REYES
College of Agriculture, Foods, and Nutrition, Universidad San Francisco
de Quito, Quito, Ecuador
The prospective cohort study examined whether Ecuadorian
women with early pregnancy nausea and vomiting (NVP) are
more likely to develop food aversions and cravings, and if so,
whether the specific foods identified as aversive or craved are the
same as those predicted by the popular maternal-embryo protection
hypothesis (MEPH). Consistent with MEPH predictions, women
Support for this study was provided by the Interamerican Development Bank and
Ecuadorian National Science and Technology Foundation (BID-FUNDACYT-234).
Address correspondence to Dr. M. Margaret Weigel, Human Nutrition and Immunology
Research Laboratory, Department of Public Health Sciences, College of Health Sciences,
University of Texas at El Paso, 1101 North Campbell St., El Paso, TX 79902-0581, USA. E-mail:
mmweigel@utep.edu
197
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
198 M. M. Weigel et al.
with NVP were more likely to report increased odor sensitivity and
aversions for some predicted “toxic” foods and more likely to crave
fruits. However, other hypothesis predictions were not supported.
The relationship of food aversions and cravings with NVP appears
more complicated than that explained by the MEPH.
KEYWORDS morning sickness, maternal-embryo protection
hypothesis, food aversions, food cravings, pica
INTRODUCTION
Women from diverse global populations often report a number of uncom-
fortable or disconcerting somatic symptoms during early gestation. These
include food aversions and cravings (Nyaruhucha 2009; Bayley et al. 2002;
Crystal, Bowen, and Bernstein 1999; Wijewardene, Fonseka, and Goonaratne
1994; Tiersen, Olsen, and Hook 1985; Dickens and Trethowan 1971), nausea
and vomiting or “morning sickness,” (Latva-Pukkila, Isolauri, and Laitinen
2010; Khresheh 2010; Nyaruhucha 2009; Lacasse et al. 2009; Chan et al.
2011; Kohl, Kainer, and Schiefenhovel 2009; Tierson, Olsen, and Hook
1986), and increased olfactory and gustatory sensitivity (Nordin et al. 2007;
Nordin, Broman, and Wulff 2005; Swallow et al. 2005; Knox, Kremer, and
Pearce 1994).
The etiology of these symptoms remains uncertain but their tempo-
ral closeness has led to speculation that they may share a common origin.
For example, Hook (1976a, 1976b, 1980) hypothesized that early pregnancy
nausea and vomiting (NVP), food aversions, and increased somatosensory
sensitivity evolved together as a symptom complex that causes pregnant
women to avoid or expel strong-smelling or strong-tasting foods containing
potentially toxic dietary abortifacents and teratogens. Although the “embryo
protection hypothesis” mainly focused on prenatal alcohol and caffeine aver-
sions, Hook also suggested that pregnant women may reject certain meats,
fried foods, oregano, and onions for the same reason.
Profet (1988, 1992, 1995) expanded on Hook’s original hypothesis. She
proposed that women who develop “pregnancy sickness” (i.e., NVP and
food aversions) are more likely to develop aversions for certain “toxic” plants
that reportedly contain high levels of potential abortifacent or teratogenic
phytochemicals such as bitter/pungent vegetables and herbs, potatoes, and
spicy/hot foods. She also proposed that fried, grilled, or roasted foods would
be the targets of aversions because their strong odors signal the presence of
potentially mutagenic compounds. She further suggested that that women
with pregnancy sickness would be less likely to reject less toxic foods char-
acterized by bland odors, mild taste, and decreased spoilage rates such as
breads, grains, cereals, and other starchy carbohydrates.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 199
Other authors subsequently extended the hypothesis, renaming it the
“maternal–embryo protection hypothesis.” They explicitly linked NVP with
the development of taste aversions through which pregnant women learn to
avoid and/or expel (vomit) animal foods such as meat, poultry, fish/seafood,
and eggs (Flaxman and Sherman 2000; Fessler 2002). The authors hypoth-
esized that these types of highly perishable foods prior to refrigeration
would have been highly subject to contamination with pathogenic microbes
and thus, consumption of such contaminated foodstuffs would have been
dangerous for pregnant women and their developing embryos.
Increased maternal sensitivity during early pregnancy to both cooked
and spoiled foods, certain spices, vinegar, alcohol and other strong-smelling
substances (e.g., cigarette smoke) has been documented in two recent stud-
ies (Nordin et al. 2005; Nordin et al. 2007). The authors hypothesized that
NVP is responsible for the formation of food and other odor aversions during
early pregnancy through classical conditioning (Nordin et al. 2007).
Another part of Hook’s (1976a, 1976b) original hypothesis addressed
prenatal food cravings. He suggested that these form part of the larger
embryo protection symptom complex and result from altered maternal
somatosensory sensitivity associated with NVP. However, different from aver-
sions, he hypothesized that food cravings act to promote maternal intake of
beneficial foods. Bayley and coauthors (2002) have suggested that prenatal
food cravings may represent conditioned responses caused by eating certain
types of foods to help relieve NVP symptoms.
The maternal-embryo hypothesis has been widely diffused through-
out the anthropological, clinical, and biological literature as well as popular
press. However, the support cited in its favor is based on circumstantial evi-
dence from population-level analyses of staple food patterns and reported
NVP presence/absence in selected societies obtained from historical ethno-
graphical reports (Minturn and Weiher 1984; Flaxman and Sherman 2000)
and population food balance estimates (Pepper and Roberts 2006). This type
of evidence is highly subject to ecological fallacy and other forms of bias.
The scarcity of relevant empirical data from contemporary populations
has made it difficult to prove or refute the maternal-embryo protection
hypothesis and the clinical advice given by some of its proponents. For
example, Profet (1992, 1995) advised that women with little or no pregnancy
sickness might want to restrict their intake of certain “embryotoxic” foods in
order to mimic the dietary behavior of others with more intense symptoms.
She also suggested that it may be counterproductive to treat mild-moderate
NVP symptoms since pregnant women would then lack a somatic guide to
help them avoid or expulse potentially dangerous foods.
Some women also develop pica during early pregnancy (Saunders
et al. 2009; Simpson et al. 2000). Such persistent or intense cravings for
non-food substances have been hypothesized to result from “olfactory
craving” (Cooksey 1995), other sensory attractions, and/or vitamin/mineral
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
200 M. M. Weigel et al.
deficiencies (Simpson et al. 2000). The potential link between NVP and
gestational pica has not been previously examined. However, it seems rea-
sonable to suggest that if women with NVP are more likely to develop
aversions for strong-flavored and strong-smelling foods or other items
(e.g., tobacco smoke, perfume), then they also should be less inclined to
develop oral cravings for substances characterized by strong somatosensory
characteristics denoting a high potential for fetotoxicity and/or micro-
bial contamination (e.g., paint chips, cement, soil, mothballs, matches,
weeds).
The present study examined the prevalence of early prenatal food aver-
sions and cravings, pica, and other somatic symptoms (i.e., perceived odor
sensitivity, appetite changes) in a large prospective cohort of women living
in Quito, Ecuador. The study also investigated the major predictions and a
logical extension of the maternal-embryo protection hypothesis. It specifi-
cally explored the question of whether women who experience NVP are
more likely to develop food aversions, heightened odor sensitivity, appetite
changes, food cravings, or pica during the first 20 weeks of gestation com-
pared to women who do not have NVP. In addition, the study examined
whether certain foods identified by pregnant women as aversive or as some-
thing they craved varies by NVP status, and if so, whether these foods are
the same as those predicted in the hypothesis.
The highland urban Ecuadorian population is apropos for the empiri-
cal study of the maternal-embryo protection hypothesis for several reasons.
The diet is rich in many of the hypothesized “toxic” foods such as pota-
toes, cruciferous vegetables, and meats, fish/seafood, poultry, and eggs (Gil
Ramos et al. 1998; Weigel, Narvaez, and Lopez 1991). In addition, onions,
garlic, oregano, cilantro, cumin, black pepper, and chile (aji) are core spices.
Frying, grilling and roasting are common food preparation methods. Food-
borne illnesses caused by microbial contamination of foodstuffs also are
endemic (Pan American Health Organization 2008).
METHODS
Study Design and Population
The study was part of a larger epidemiological investigation that exam-
ined the association of NVP and other maternal factors with fetal outcome
in a prospective cohort of women living in Quito, the capitol city of
Ecuador (Weigel et al. 2006). The city is located in the Andean highlands
of northern Ecuador at an elevation of approximately 2,800 meters above
sea level (Distrito Metropolitano de Quito [DMQ] 2008). Ecuador’s demo-
graphic transition during the past two decades has transformed it from a
rural, agrarian society to one where two-thirds of the country’s population
now lives in congested urban centers such as Quito (Central Intelligence
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 201
Agency 2010). Quito’s estimated two million inhabitants are relatively young.
Nearly six-tenths are under the age of 30 years (DMQ). Mestizos (i.e., per-
sons of mixed Spanish and indigenous ancestry) are the predominant ethnic
group, followed by Quechua indigenous groups, Afro-Ecuadorians (Centro
de Estudios de Población y Desarrollo Social [CEPAR] 2005; DMQ). Most
pregnant and other reproductive-aged women living in the Quito area have
completed at least some years of secondary education (Weigel et al. 2000;
CEPAR). The large majority of women in Quito receive at least some for-
mal prenatal care (86.3%) during their pregnancies from a public or private
health care facility. Seventy-three percent have first prenatal visit as early as
the first trimester (CEPAR).
Study Participants
The data were collected from a consecutive sample of 849 women attend-
ing the prenatal clinics of a public city hospital, Hospital Municipal San
Jose de Quito. The facility is located in the south of Quito and serves a
predominantly working class population. Healthy women with a singleton
pregnancy who were in their first trimester, who planned to have all prenatal
care and labor/delivery at the same institution, and had resided in Quito for
at least six months prior to conception were eligible for study participation.
Prospective participants were excluded if their medical history or physical
examination revealed a serious health condition or the use of medications
or drugs that could adversely affect pregnancy outcome. All prospective
participants went through the informed consent process and provided their
written consent before enrollment. The study protocol was approved by the
research committee of the host medical institution and the Universidad San
Francisco de Quito medical ethics committee.
Data Collection
A structured questionnaire with open- and closed-ended items was used to
collect data on participant sociodemographic, reproductive, environmental,
and lifestyle characteristics. Other questions asked study participants as to
whether or not they had experienced any nausea or vomiting since their last
menstrual period, and if so, the timing, peak and duration of these symp-
toms. Women who reported nausea and/or vomiting solely in conjunction
with diarrhea, fever, and/or chills were presumed to have gastroenteritis
unless nausea and/or vomiting, in the absence of gastroenteric symptoms,
were also recorded at another prenatal visit during the first 20 weeks of ges-
tation. In addition, participants were asked whether they had developed any
food aversions, changes in somatosensory sensitivity or appetite (reduced or
increased), food cravings, pica, or other somatic symptoms since becoming
pregnant.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
202 M. M. Weigel et al.
In this study, a food aversion was defined as a strong negative response
to a particular food or beverage that was not disliked prior to pregnancy.
Food cravings and pica were defined as a strong urge to consume a
food/beverage or a non-food substance, respectively, for which there had
not been an intense desire prior to their current pregnancy. Women who
reported any food aversions, food cravings, or pica were then asked to detail
them using the free-list method. In addition, they were questioned about
what they believed had caused these and whether, in fact, they had actually
avoided or consumed the desired items. The questionnaire was administered
in face-to-face interviews with participants by trained study interviewers dur-
ing the initial first trimester prenatal visit (11.1 ±3.7 weeks). It was repeated
again at a subsequent prenatal visit at gestation weeks 24–28.
Data Analysis
The association of NVP with aversions reported for specific foods was ana-
lyzed from the free-listings provided by the participants. Several categories
of food aversions emerged from their responses. The frequency of foods in
each of the food categories was divided by the total sum of all specified food
aversions or alternatively, cravings, in order to produce the descriptive per-
centages described in the text. However, since this tabulation method can
result in pseudo-replication, a subject response was recorded as positive
if she reported at least one aversion for a food in that particular category
and negative if none were mentioned (Tierson et al. 1985). For example,
if a subject reported aversions for both broccoli and cabbage, they were
listed as positive for a bitter and pungent vegetable aversion. Each food
was counted only once. They were categorized according to the description
given by a participant for that food. For example, if a participant reported
aversions for fried meat, they were listed as positive for fried/grilled/roasted
foods. The same methodological approach was used to analyze cravings
for foods and non-food items (gestational pica) reported by the pregnant
participants.
Descriptive data were analyzed as frequencies with percents or means
with standard deviations. To examine the hypothesized association of NVP
with food aversions, somatosensory sensitivity, appetite changes, food crav-
ings, and pica, participants were divided into ordinal categories according
to the most severe level of NVP they reported experiencing during the first
20 weeks of gestation. These levels were no NVP symptoms, nausea only,
or nausea accompanied by vomiting. Mean differences were assessed using
Students’ unpaired ttests or ANOVA, as appropriate. Contingency table anal-
ysis with χ2was used to investigate differences between proportions. This
bivariate method also was used to calculate the unadjusted odds ratios and
95% confidence intervals (CI). Multiple logistic regression analysis (simulta-
neous entry, no variable elimination) was used to produce an adjusted odds
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 203
ratio and 95% CI for each factor of interest, taking into account the influence
of potential confounders.
RESULTS
Participant Characteristics
Table 1 displays the sociodemographic, reproductive, environmental and
other characteristics of the 849 study participants. A majority were under
the age of 30 years, legally married, multiparous, and full-time housewives.
Most women reported that they had completed at least some middle or
high school education and nearly one-third had some post-secondary educa-
tion or technical training (e.g., cosmetology, secretarial school, accounting).
The others reported that they were currently employed in either blue or
TABLE 1 Subject Characteristics (N=849)
Subject characteristics n(%)
Ethnicity: Mestizo 844 (99.4)
Maternal age
≤20 years 118 (11.8)
20–24 years 272 (32.0)
25–29 years 220 (25.9)
≥30 years 239 (28.2)
Marital status: in union 742 (87.4)
Formal education: years completed
≤6 years 55 (6.5)
7–9 years 125 (14.7)
10–12 years 410 (48.3)
Post-secondary technical or other
training/education
259 (30.5)
Primary occupation
Full-time housewife 528 (62.2)
Blue collar/tradesperson 167 (19.7)
White collar/professional 102 (12.0)
Student 49 (5.8)
Number of dependents presently living
in home
3.49 ±1.7
Housing
Own house or apartment 287 (33.8)
Rent house or apartment 451 (53.1)
Other: live with relatives, friends, or
employer as domestic servant
107 (12.6)
Home characteristics
Electricity 845 (99.5)
Piped in water 833 (98.1)
Inside toilet 733 (86.3)
Parity: Primipara 363 (42.8)
Current pregnancy planned 382 (45.0)
Any periconceptual cigarette smoking 12 (1.4)
Any periconceptual alcohol use 83 (9.8)
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
204 M. M. Weigel et al.
white-collar professions or were attending school. Four-tenths of the par-
ticipants were primiparas. Only 45% said that their current pregnancy was
planned. Fewer than 10% reported smoking any cigarettes or consuming
alcoholic beverages in the periconceptual period.
Nausea and Vomiting
Early-pregnancy nausea and vomiting affected 77.3% (654/849) of the study
participants. One-fifth (21.1%; 179/849) experienced nausea only and 56.2%
(475/849), both nausea and vomiting. The average onset of symptoms was
6.1 ±2.5 weeks (nausea) and 6.5 ±2.7 weeks (vomiting). Symptoms peaked
in intensity during gestation week 10. They gradually diminished so that by
week 20, only 3.4% reported any NVP.
Thirty-nine percent (256/654) of women with NVP reported that they
had tried one or more self-treatments to manage their NVP symptoms. The
single most frequently reported method used (55.3%; 175/318 responses)
involved “food therapy” such as sucking on or eating tart or sweet fruits,
drinking heavily iced beverages, frequent eating to keep the stomach full,
avoiding problematic foods, and skipping breakfast. Behavioral changes
such as frequent resting in a supine position, deep breathing, self-induced
vomiting, “aroma therapy” (e.g., sniffing fresh fruit, flowers, rubbing alcohol,
cologne) or aroma avoidance (staying out of the kitchen, avoiding provoca-
tive odors) accounted for another 13.2% (42/318) of mentioned methods.
The remainder involved the use of vitamin–mineral supplements (5.8%;
18/318), antacids (8.2%; 26/318), and anti-emetic drugs (17.9%; 57/318) such
as scopolamine ormetochlopramide.1
Food Aversions, Increased Odor Sensitivity, and Reduced Appetite
Three-quarters of the 849 participants reported developing one or more
food aversions (73.6%; 625/849) during the first half of pregnancy or height-
ened odor sensitivity (75.9%; 644). Slightly more than half (54.4%; 462) also
reported that they had experienced reductions in their appetite since becom-
ing pregnant. A total of 1,413 food aversions were identified by the study
participants using the free-listing method. These formed 12 natural cate-
gories. Nearly half (46.1%; 651) of the food aversions reported by pregnant
women were for various meats (e.g., beef, pork, lamb, liver/other organs,
hot dogs, sausage, guinea pig), poultry (e.g., chicken), fish (e.g., tilapia,
seabass, tunafish), seafood (e.g., shrimp, prawns, squid), and chicken or
quail (codorniz) eggs. Thirteen percent (13.3%; 197) of reported aversions
were for “toxic vegetables” such as cabbage, cauliflower, broccoli, Brussels
1Generic name for prescription medications used to treat nausea and vomiting symptoms caused by
a variety of conditions.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 205
sprouts, onions, eggplant, tomatoes, turnip greens, potatoes, and mellocos,
an indigenous potato-like tuber.
White rice, wheat noodles, corn, barley, and other starchy carbohydrate
foods accounted for 12.8% (181) of the identified food aversions and foods
prepared by frying, roasting, or grilling for another 9.2% (130). Spicy/hot
foods such as garlic, cumin, oregano, curry, cilantro, chile peppers, and
black pepper accounted for 8.5% (120) of food aversions.
The other food categories accounted for fewer than 5% each of the
aversions reported. These included milk/other dairy foods, such as yogurt and
cheese (3.1%; 44), all other (non-toxic) vegetables/legumes (1.9%; 27) such
as beets, squash, avocado, lentils, green peas, fruits and fruit juices (1.5%; 21),
caffeinated beverages/foods (1.4%; 20), and “sweets” (.8%; 12). The final two
free-list food-aversion categories were alcoholic beverages (.01%; 2) and foods
described only as having salty and liquid attributes (.05%; 8).
Consistent with predictions, women with NVP were more likely than
those without any NVP to report that since becoming pregnant, they had
developed increased odor sensitivity and food aversions including those for
at least one of the foods hypothesized as toxic or harmful (table 2). They
also were more likely to report experiencing a reduction in appetite which
contrasts with women without any NVP who more often indicated that their
appetite had significantly increased since becoming pregnant (AOR =1.77;
95% CI 1.28, 2.45).
Women who experienced nausea only or both nausea and vomiting
reported a greater average number of food aversions compared to their
non-NVP counterparts (¯
x=2.0 ±.96 vs. 2.2 ±.89 vs. 1.85 ±.99 aversions;
F=6.54; p=.002). As figure 1 shows, a significantly greater proportion
of women with than without NVP reported aversions for four of the spe-
cific “harmful” food categories predicted by the maternal-embryo protection
hypothesis: meat, poultry, fish/seafood and eggs, potatoes and other “toxic”
vegetables and potatoes, spicy/hot foods and fried/roasted/grilled foods.
However, different from hypothesis predictions, participants who had NVP
were more, not less, likely to report aversions for starchy carbohydrate foods
hypothesized to have a low “toxicity” potential. No statistically significant
between-group differences were identified in the proportion of participants
who reported aversions for alcohol and caffeinated items. The single most
frequent explanation given by the participants who developed food aver-
sions for these was the disagreeable odor of the food(s) in question (73%).
The other explanations reported were unpleasant food appearance (6.9%),
taste (5.3%) or texture (3.2%).
Food Cravings
Sixty-nine percent (590/849) of women reported that they had developed
a craving for at least one food during the first 20 weeks of gestation.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
206 M. M. Weigel et al.
TABLE 2 Association of NVP with Food Aversions, Increased Odor Sensitivity, Reduced
Appetite, Food Cravings, and Pica Reported during the First 20 Weeks of Gestation (N=849)
Unadjusted odds Adjusted odds
Symptoms No. (%) ratio (95% CI) ratio (95% CI)a
Any food aversion
Nausea with vomiting 400 (84.2) 7.70 (5.27, 11.3) 7.40 (4.97, 11.0)
Nausea only 146 (80.7) 6.02 (3.77, 9.61) 5.86 (3.64, 9.45)
No NVP 79 (40.9) 1.00 (referent) 1.00 (referent)
Aversions for >1
hypothesized “harmful”
foodsb
Nausea with vomiting 339 (71.4) 4.58 (3.21, 6.54) 4.36 (3.00, 6.31)
Nausea only 122 (67.4) 3.80 (2.48, 5.84) 3.67 (2.36, 5.70)
No NVP 68 (35.2) 1.00 (referent) 1.00 (referent)
Increased sensitivity to odors
Nausea with vomiting 393 (82.7) 3.21 (2.20, 4.67) 3.08 (2.08, 4.55)
Nausea only 136 (75.1) 2.02 (1.30, 3.15) 1.95 (1.24, 3.07)
No NVP 115 (59.9) 1.00 (referent) 1.00 (referent)
Reduced appetite
Nausea with vomiting 303 (63.8) 3.47 (2.44, 4.93) 3.48 (2.41, 5.02)
Nausea only 94 (51.9) 2.13 (1.40, 3.23) 2.10 (1.36, 3.22)
No NVP 65 (33.7) 1.00 (referent) 1.00 (referent)
Any food craving
Nausea with vomiting 337 (70.9) 1.79 (1.22, 2.45) 1.77 (1.23, 2.56)
Nausea only 134 (74.0) 2.02 (1.30, 3.13) 1.97 (1.25, 3.10)
No NVP 113 (58.5) 1.00 (referent) 1.00 (referent)
Any pica
Nausea with vomiting 18 (3.8) 3.76 (.86, 16.4) 3.68 (.82, 16.1)
Nausea only 6 (3.3) 3.27 (.65, 16.4) 3.44 (.68, 17.5)
No NVP 2 (1.0) 1.00 (referent) 1.00 (referent)
Note.CI=Confidence intervals.
aMultiple logistic regression analyses adjusted for maternal age, periconceptual use of alcohol, tobacco,
and vitamin-mineral supplements, and antiemetic drugs.
b“Meats,” pungent/bitter vegetables, spicy/hot, fried/grilled/roasted, alcohol, caffeine.
Using the free-list method, they identified a total of 1,443 food cravings
that were grouped into 12 categories. Fruits and fruit juices were the sin-
gle most common food category reported, accounting for 35.6% (514) of all
cravings. Twenty-seven different types of fruits were mentioned, the most
frequent of which were limes, apples, oranges, grapes, pineapple, tanger-
ines, watermelon, mangoes, and strawberries. Nearly one-fifth (19.2%; 277)
of the reported food cravings were for meats, poultry, fish/seafood and
eggs. Starchy carbohydrate foods (8.3%; 119), fried/grilled/roasted foods
(6.7%; 96), milk/other dairy foods (6.3%; 91), and “toxic vegetables” (5.5%;
80) comprised fewer than one-tenth of the reported craved items. Fewer
than five percent reported cravings for “sweets” (4.7%; 68), caffeinated
beverages/foods (4.3%; 62), “non-toxic” vegetables/legumes (3.8%; 55),
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 207
Percent
No NVP (193)
Nausea only (181)
Nausea & vomiting (475)
Meat/poultry, fish & eggs∗
Starchy carbohydrates∗
"Non-toxic" vegetables∗
"Toxic" vegetables∗
Fried/grilled/roasted foods∗∗
Spicy/hot foods∗∗∗
Salty, liquids foods∗∗∗
Milk & other dairy foods
Fruit & fruit juices
Caffeinated foods & beverages
Alcoholic beverages
70
60
50
40
30
20
10
0
Food Aversion Categories
FIGURE 1 Association of the nausea and vomiting of early pregnancy (NVP) with reported
maternal food aversions (N=849). ∗p=.0001; ∗∗p=.008; ∗∗∗p<.02; all other food
categories, p≥.05 (color figure available online).
salty, liquid foods (3.3%; 48), spicy/hot foods (2.1%; 31), and alcoholic
beverages (.06%; 2).
Women who experienced NVP, especially those who had only nausea,
were more likely to report early prenatal cravings compared to those without
any NVP (table 2). However, as figure 2 shows, this difference was almost
entirely due to cravings for fruits as no statistically significant between-group
differences were identified for other food categories. No statistically signifi-
cant between-group differences were identified regarding the mean number
of food cravings reported by women with nausea only, nausea with vomit-
ing,andnoNVP(
x=2.6 ±1.1 cravings vs. 2.0 ±.9 cravings vs. 1.9 ±1.1
cravings; F=1.0; p=.37).
Ninety-five percent (561/590) of the women who developed any early
prenatal food cravings indicated that they had been able to obtain and con-
sume the target food(s). Sixty-five percent reported that they knew why
they had developed these. Different from what they reported for food aver-
sions, most participants (80.5%) identified the attractive taste of the craved
food(s) in question as responsible for their cravings. Only a few mentioned
that their cravings had been invoked by the particular smell (8%) or visual
appeal (11%) of specific foods.
Gestational Pica
The overall prevalence of pica reported by participants during the first
20 weeks of gestation was 3.1% (26/849). No statistically significant between-
group differences were identified between women with and without NVP
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
208 M. M. Weigel et al.
Percent
No NVP (193)
Nausea only (181)
Nausea & vomiting (475)
Meat/poultry, fish & eggs
Starchy carbohydrates
"Non-toxic" vegetables
"Toxic" vegetables
Fried/grilled/roasted foods
Sweets
Other
Milk & other dairy foods
Fruit & fruit juices∗
Caffeinated foods & beverages
Alcoholic beverages
50
45
40
35
30
25
20
15
10
0
5
Food Craving Categories
FIGURE 2 Association of the nausea and vomiting of early pregnancy (NVP) with reported
maternal food cravings (N=849). ∗fruits: p=.024; all other food categories: p≥.05 (color
figure available online).
(table 2). The items most frequently reported as craved by women with pica
were laundry detergents and soaps (28.6%), black soil (14.3%), phosphorous
matches (9.5%), cement block crumbs (4.8%), old shoe leather (4.8%),
latex house paint (4.8%), hand lotion (4.8%), and weeds (4.8%). None
reported any cravings for clay. Seventy-nine percent of the 26 participants
who reported pica said that they were able to explain their cravings. Most
attributed these to the “attractive” odor (66.7%) or taste (26.7%) of the target
items. The remainder (6.6%) indicated that it was for other reasons such as
appearance or color.
DISCUSSION
The sociodemographic, reproductive, and lifestyle characteristics of the
study participants were representative of those reported for Quito women of
reproductive age (15–49 years) in the national demographic and maternal-
infant health survey (CEPAR 2005). The overall prevalence and temporal
pattern for NVP in our study were comparable with those reported for
Ecuadorian women at a public maternity hospital in Quito (Weigel et al.
2000) and others in Jordan (Khresheh 2010), Finland (Latva-Pukkila et al.
2010), Tanzania (Nyaruhucha 2009), Canada (Lacasse et al. 2009), the United
States (Chan et al. 2011), and Guatemala, South Africa, and Germany (Kohl
et al. 2009).
The lack of published data on prenatal food aversions and crav-
ings does not permit comparison with other Ecuadorian groups. However,
the prevalence of food aversions and cravings identified in the current
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 209
work was comparable that reported for pregnant women from diverse
global populations such as Tanzania (Nyaruhucha 2009), Ethiopia (Demisse,
Muroki, and Kogi-Makau 1998), Sri Lanka (Wijewardene 1994), Great Britain
(Bayley et al. 2002) and the U.S. (Crystal et al. 1999; Tiersen et al. 1985). The
close cross-cultural agreement lends support to the notion that these three
common symptoms have a physiological basis.
The general classes of foods that the pregnant Ecuadorian study par-
ticipants found particularly aversive or especially craved were consistent
with the cross-cultural data from other contemporary empirical studies.
However, like these, many of the specific fish/meat (e.g., roasted whole
guinea pig, ceviche,2guatita,3or tripa misqui4), tubers (e.g., mellocos
[Ullucus tuberosus],seeds (e.g., chochos [Lupinus mutabilis], grains (quinoa
[Chenopodium quinoa]) fruits (e.g., naranjilla [Solanum quitensis], chrimoya
[Annona Cherimola]), and other foods and food dishes identified as the tar-
get of prenatal aversions or cravings were indigenous to Ecuador and the
larger Andean highland region.
The study findings were consistent with several of the maternal–
embryo protection hypothesis assumptions concerning food aversions. For
example, as predicted, women who had nausea either with or without
vomiting were 6–7 times more likely than those without NVP to report
they had developed increased odor sensitivity and aversions for at least
one of the hypothesized types of harmful foods, especially meat, poultry,
fish/seafood, and eggs, “toxic” (bitter/pungent) vegetables, spicy/hot foods,
and fried/roasted/grilled foods. Also consistent with the hypothesis, most
women identified a strong/disagreeable odor as the primary trigger for their
food aversions.
Other aversion-related predictions were not supported by the study
data. For instance, women with NVP were more, not less likely to report
developing aversions during early gestation for polished rice, corn, green
plantains, quinoa, and other common starchy carbohydrate foods proposed
to have a low toxicity potential (Profet, 1988, 1992, 1995). Many of these are
staple foods in the Ecuadorian diet (Weigel et al. 1991; Weigel et al. 1992; Gil
Ramos et al. 1998). Similar aversions to starchy staple foods also have been
reported for pregnant women living in other societies (Nyaruhucha 2009;
Demisse et al. 1998). The explanation for the development of this aversion
is not immediately evident.
One proximate level explanation might be that the combination of NVP
and heightened odor sensitivity may evoke conditioned responses even for
frequently eaten, familiar foods (Coad et al. 2002) such that which occurs
during cancer chemotherapy (Aisner 2007). Another possibility is that this
food group is not necessarily as innocuous as assumed by some hypothesis
2Raw seafood or fish with chopped onions, cilantro, and tomatoes, marinated in key lime juice.
3Boiled tripe in peanut sauce.
4Grilled cow intestines.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
210 M. M. Weigel et al.
proponents. Many of these foods were manipulated genetically by humans
during the last 10,000 years. Mycotoxin contamination of fresh and stored
rice, corn, wheat and other grains is common worldwide (Tanaka et al. 1998)
and was probably even more so in the distant past when humans began
storing food. Maternal exposure to relatively small doses of mycotoxins has
been linked with miscarriage and birth defects (Missmer et al. 2006; Peraica
et al. 1998).
The hypothesized link between NVP and alcohol and caffeine aversions
was not supported by the study data. However, some caution is warranted
regarding the interpretation of these results as the relatively low prevalence
of both may have affected our ability to detect any between-group differ-
ences, if present. The prevalence of prenatal alcohol and caffeine aversions
is reported to vary widely across populations. The low frequency of pre-
natal alcohol consumption reported in the study was comparable to figures
reported for some pregnant groups in Quito (Weigel et al. 2000), Ethiopia
(Demisse et al. 1998), Italy (Alberti-Fidanza et al. 1996) and U.S. (Tierson
et al. 1985) but reduced compared to others in the latter country (Hook
1976; Lawson et al. 2004). The reason for these differences is not imme-
diately evident but could be due to methodological or culturally based
distinctions related to the frequency of these items in the general diet and
whether they are seen as something that women should or should not con-
sume. For example, alcoholic beverage consumption during pregnancy in
Ecuador is generally frowned upon except for the occasional toast during
social events with an ounce or less of fermented plantain “champagne” or
occasional beer-egg mixture drunk during late pregnancy to improve future
breastmilk production (unpublished data). Likewise, the caffeine content
of the Ecuadorian diet is relatively low (Gil Ramos et al. 1998; Weigel
et al. 1992). The most commonly consumed caffeinated items are cola-
type beverages or café en leche. The latter consists of a small teaspoon
of instant coffee dissolved in a cup of heavily sweetened warm milk which
lacks the strong aroma and bitter taste usually associated with the brewed
product.
Consistent with the maternal-embryo protection hypothesis, women
with NVP were more likely to develop food cravings compared to those
without NVP symptoms. However, the strength of the association was
reduced compared than that observed for food aversions and mostly
accounted for by cravings for only type of food (i.e., fruits). Also differ-
ent from aversions, most of the study women attributed their cravings to the
attractive taste rather than smell of the target foods. In addition, half of the
women who had NVP said that they used “food therapy” to control their
symptoms.
These findings lend support to the notion that prenatal dietary cravings
may represent conditioned responses caused by eating foods to allevi-
ate NVP symptoms (Bayley et al. 2002) or to counteract the negative
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 211
physiological effects of frequent vomiting (e.g., hypoglycemia, blood elec-
trolytes). This could also help to clarify why some women develop cravings
for certain types of nutrient-rich foods (e.g., meat and eggs) hypothesized
as “toxic” by the maternal-embryo protection hypothesis. However, it does
not account for why nearly six-tenths of women without any NVP symptoms
also developed food cravings.
The frequency of persistent or intense cravings for non-food items
(gestational pica) among the study participants was low but within the
wide 0–68% range reported for pregnant women at various gestational
stages. The major objects of their cravings also were similar such as strong-
smelling/tasting detergents and soaps, soil, matches, cement chips (Simpson
2000). However, different from the a priori prediction, no association was
identified between NVP and decreased risk for developing pica during early
gestation. It is possible that the reported frequency of gestational pica in
the Ecuadorian sample was too low to permit meaningful statistical analysis.
This issue requires further study in populations with higher gestational pica
prevalence.
In conclusion, the empirical data from this study suggest that the
relationship among food aversions, cravings, and NVP appears more com-
plicated than that explained by the maternal-embryo protection hypothesis.
The application of other aspects of this hypothesis in clinical practice is pre-
mature and could lead to symptom under-treatment or decreased dietary
diversity or quality (Badell et al. 2006; Brown et al. 1997).
Although the cross-cultural evidence indicates that women who develop
NVP have a significantly reduced risk for miscarriage (Weigel et al. 2006),
additional population-based prospective cohort studies conducted in diverse
cultural settings are needed before the maternal-embryo protection hypoth-
esis can be conclusively refuted or supported. In particular, the effect of
food aversions and cravings on the early prenatal diet should be investi-
gated. This is an important issue since emerging human and animal evidence
including indicates that maternal energy intake, the macronutrient compo-
sition of the diet (Metges 2009; Kind et al. 2006), and ingestion of some
micronutrients (Cetin, Berti, and Calabrese 2010; Mathews, Yudkin, and
Neil 1999) during early gestation can influence placental growth and func-
tion, modify fetal physiology, and/or influence postnatal development of
obesity and chronic diseases such as diabetes, hypertension, asthma and
atopy.
ACKNOWLEDGMENTS
The authors acknowledge the excellent technical assistance of Obst. Sara
Cespedes, Dr. Sylvia Duchicela, Dr. Miriam Betancourt, and the medical staff
of the Hospital Patronato Municipal San Jose.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
212 M. M. Weigel et al.
REFERENCES
Alberti-Fidanza, A., A. Maurizi Coli, I. Ottavi, and W. Panarelli. 1996. Nutritional
studies on pregnant women in Umbria (Italy). Bibliotheca Nutritio Et Dieta
53:11–22.
Aisner, J. 2007. Overview of the changing paradigm in cancer treatment: Oral
chemotherapy. American Journal of Health-System Pharmacy 64:S4–S7.
Badell, M. L., S. M. Ramin, and J. A. Smith. 2006. Treatment options for nausea and
vomiting during pregnancy. Pharmacotherapy 26:1273–1287.
Bayley, T. M., L. Dye, S. Jones, M. DeBono, and A. J. Hill. 2002. Food cravings and
aversions during pregnancy: Relationships with nausea and vomiting. Appetite
38:45–51.
Brown, J. E., E. S. Kahn, and T. J. Hartman. 1997. Profet, profits, and proof: Do nau-
sea and vomiting of early pregnancy protect women from “harmful” vegetables?
American Journal of Obstetrics and Gynecology 176:179–181.
Central Intelligence Agency (CIA). 2010. World factbook, 2010, Ecuador. https://
www.cia.gov/library/publications/the-world-factbook/geos/ec.html (accessed
September 28, 2010).
Centro de Estudios de Población y Desarrollo Social (CEPAR). 2005. Encuesta
Demográfica y de Salud Materna e Infantil (ENDEMAIN 2004). Quito,
Ecuador: CEPAR. http://www.cepar.org.ec/endemain_04/nuevo05/provincia/
indice_p.htm (accessed October 5, 2010).
Cetin, I., C. Berti, and S. Calabrese. 2010. Role of micronutrients in the periconcep-
tional period. Human Reproduction Update 16 (1): 80–95.
Chan, R. L., A. F. Olshan, D. A. Savitz, A. H. Herring, J. L. Daniels, H. B. Peterson,
and S. L. Martin. 2011. Maternal influences on nausea and vomiting in early
pregnancy. Maternal and Child Health Journal 15 (1): 122–127.
Coad, J., B. Al-Rasai, and J. Morgan. 2002. Nutrient insult in early pregnancy.
Proceedings of the Nutrition Society 61:51–59.
Cooksey, N. R. (1995. Pica and olfactory craving of pregnancy: How deep are the
secrets? Birth 22 (3):129–137.
Crystal, S. R., D. J. Bowen, I. L. Bernstein. 1999. Morning sickness and salt intake,
food cravings, and food aversions. Physiology and Behavior 67:181–187.
Demisse, T, N. M. Muroki, and W. Kogi-Makau. 1998. Food aversions and crav-
ings during pregnancy: Prevalence and significance for maternal nutrition in
Ethiopia. Food and Nutrition Bulletin 19:20–26.
Dickens, G., and W. H. Trethowan. 1971. Cravings and aversions during pregnancy.
Journal of Psychosomatic Research 15:259–268.
Distrito Metropolitano de Quito (DMQ). 2008. Comisión de Equidad Social y Género
MDMQ, Gestión Margarita Carranco. Quito, Ecuador: DMQ. http://www.pro
casur.org/fida/documentos/CASO%20Quito.pdf (accessed October 10, 2010).
Fessler, D. M. 2002. Reproductive immunosupression and diet: An evolutionary per-
spective on pregnancy sickness and meat consumption. Current Anthropology
43:19–61.
Flaxman, S. M., and P. W. Sherman. 2000. Morning sickness: A mechanism for
protecting mother and embryo. Quarterly Review of Biology 75:113–148.
Gil Ramos, J., H. Dirren, L. Layedra, N. Condor, T. Benavides, and J. O.
Mora. 1998. Consumo de Alimentos en el Primer Trimestre de Gestacion en
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
NVP, Food Aversions, and Cravings 213
Barrios Suburbanos del Norte de Quito. Quito, Ecuador: Nestlé Research and
Development Center.
Hook, E. B. 1976a. Changes in tobacco smoking and ingestion of alcohol and caf-
feinated beverages during early pregnancy: Are these consequences, in part, of
feto-protective mechanisms diminishing maternal exposure to embryotoxins? In
Birth defects, ed. S. Kelly, 173–183. New York: Academic Press.
Hook, E. B. 1976b. Dietary cravings and aversions during pregnancy. American
Journal of Clinical Nutrition 31:1355–1362.
Hook, E. B. 1980. Influence of pregnancy on dietary selection. International Journal
of Obesity 4:338–340.
Kind, K. L., V. M. Moore, M. J. Davies. 2006. Diet around conception and during
pregnancy—Effects on fetal and neonatal outcomes. Reproductive Biomedicine
Online 12 (5): 532–541.
Knox, B., J. Kremer, and J. Pearce. 1994. Food fads during pregnancy: A question
of taste? Appetite 23 (3): 288.
Kohl, S., F. Kainer, and W. Schiefenhovel. 2009. Nausea and vomiting as evolutionary
mechanisms of the complex adaptation reaction to pregnancy. Zeitschrift fr
Geburtshilfe und Neonatologie 213 (5): 186–193.
Khresheh, R. 2010. How women manage nausea and vomiting during pregnancy: A
Jordanian study. Midwifery 27 (1): 42–45.
Lacasse, A., E. Rey, E. Ferreira, C. Morin, and A. Berard. 2009. Epidemiology
of nausea and vomiting of pregnancy: Prevalence, severity, determinants,
and the importance of race/ethnicity. BMC Pregnancy and Childbirth 9 (26).
doi:10.1186/1471-2393-9-26.
Latva-Pukkila, U., E. Isolauri, and K. Laitinen. 2010. Dietary and clinical impacts
of nausea and vomiting during pregnancy. Journal of Human Nutrition and
Dietetics 23 (1): 69–77.
Lawson, C. C., G. K. LeMasters, and K. A. Wilson. 2004. Changes in caffeine
consumption as a signal of pregnancy. Reproductive Toxicology 18:625–633.
Mathews, F., P. Yudkin, and A. Neil. 1999. Influence of maternal nutrition on
outcome of pregnancy: Prospective cohort study. British Medical Journal
319:339–343.
Metges, C. C. 2009. Early nutrition and later obesity: Animal models provide insights
into mechanisms. Advances in Experimental Medical Biology 646:105–12.
Minturn, L, and A. W. Weiher. 1984. The influence of diet on morning sickness: A
cross-cultural study. Medical Anthropology 8 (1): 71–75.
Missmer, S. A., L. Suarez, M. Felkner, E. Wang, A. H. Merrill, Jr., and K. J. Rothman.
2006. Exposure to fumonisins and the occurrence of neural tube defects along
the Texas-Mexico border. Environmental Health Perspectives 114:237–241.
Nordin, S., D. A. Broman, and M. Wulff. 2005. Environmental odor intolerance in
pregnant women. Physiology and Behavior 84:175–179.
Nordin, S., D. A. Broman, E. Bringlöv, and M. Wulff. 2007. Intolerance to ambi-
ent odors at an early stage of pregnancy. Scandinavian Journal of Psychology
48 (4): 339–343.
Nyaruhucha, C. N. M. 2009. Food cravings, aversions, and pica among pregnant
women in Dar es Salaam, Tanzania. Tanzanian Journal of Health Research
13 (1): 29–34.
Pan American Health Organization (PAHO). 2008. Health in the Americas.
Washington DC: PAHO.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
214 M. M. Weigel et al.
Pepper, G. V., and S. Craig Roberts. 2006. Rates of nausea and vomiting in pregnancy
and dietary characteristics across populations. Proceedings of the Royal Society
B273 (1601): 2675–2679.
Peraica, M., B. Radic., and M. Pavlovic. 1999. Toxic effects of mycotoxins in humans.
Bulletin of the World Health Organization 77:754–766.
Profet, M. 1988. The evolution of pregnancy sickness as a protection to the embryo
against Pleistocene teratogens. Evolutionary Theory 8:177–190.
Profet, M. 1992. Pregnancy sickness as adaptation: A deterrent to maternal ter-
atogens. In The adapted mind: Evolutionary psychology and the generation of
culture, ed. J. H. Barkow, 327–365. New York: Oxford University Press.
Profet, M. 1995. Protecting your baby-to-be: Preventing birth defects in the first
trimester. New York: Addison-Wesley.
Saunders, C., P de C. Padilha, B. Della Líbera, J. L. Nogueira, L. M. Oliveira,
and A. Astulla. 2009. Pica: Epidemiology and association with pregnancy
complications. Revista Brasileira de Ginecologia e Obstetrícia 31 (9): 440–446.
Simpson, E., J. D. Mull, E. Longley, and J. East. 2000. Pica during pregnancy in low-
income women born in Mexico. Western Journal of Medicine 173 (1): 20–24.
Swallow, B. L., S. W. Lindow, E. A. Masson, and D. M. Hay. 2005. Women with
nausea and vomiting in pregnancy demonstrate worse health and are adversely
affected by odours. Journal of Obstetrics and Gynecology 25:544–549.
Tanaka, T., A. Hasegawa, S. Yamamoto, U.-S. Lee, Y. Sugiura, and Y. Ueno. 1988.
Worldwide contamination of cereals by the Fusarium mycotoxins nivalenol,
deoxynivalenol, and zearalenone. 1. Survey of 19 countries. Journal of
Agricultural and Food Chemistry 36:979–983.
Tierson, F. D., C. L. Olsen, and E. B. Hook. 1985. Influence of cravings and aversions
on diet in pregnancy. Ecology of Food and Nutrition 17:117–129.
Tierson, F. D., C. L. Olsen, and E. B. Hook. 1986. Nausea and vomiting of pregnancy
and association with pregnancy outcome. American Journal of Obstetrics and
Gynecology 155:1017–1022.
Weigel, M. M., R. X. Armijos, M. H. Monaco, R. Izurieta. J. R. Racines, C. Zurita,
and G. Jaramillo. 1992. Nutritional and health status of rural women colonists
residing in Northwest Ecuador. Ecology of Food and Nutrition 29:25–43.
Weigel, M. M., M. E. Caiza, J. Lascano, G. Barreno, and L. Mosquera. 2000. The
nausea and vomiting of early pregnancy in a high-altitude Andean population.
International Journal of Gynecology and Obstetrics 69 (1): 9–21.
Weigel, M. M., W. M. Narvaez, and A. Lopez. 1991. Prenatal diet, nutrient
intake, and pregnancy outcome in an urban Ecuadorian population. Archivos
Latinoamericanos de Nutricion 26 (1): 21–37.
Weigel, M. M., M. Reyes, M. E. Caiza, N. Tello, N. P. Castro, S. Cespedes, S. Duchicela,
and M. Betancourt. 2006. Is the nausea and vomiting of early pregnancy really
feto-protective? Journal of Perinatal Medicine 34:115–122.
Weigel, R. M., and M. M. Weigel. 1989. Evaluating the association between
early pregnancy nausea and vomiting with miscarriage and perinatal mor-
tality: A meta-analytic review. British Journal of Obstetrics and Gynecology
96:1312–1318.
Wijewardene, K., P. Fonseka, and C. Goonaratne. 1994. Dietary cravings and
aversions during pregnancy. Indian Journal of Public Health 38:95–98.
Downloaded by [The University of Texas at El Paso] at 11:56 14 February 2013
