http://cpj.sagepub.

com/
Clinical Pediatrics
http://cpj.sagepub.com/content/52/3/241
The online version of this article can be found at:

DOI: 10.1177/0009922812472250
2013 52: 241 originally published online 24 January 2013 CLIN PEDIATR
Daiva Gorczyca, Anna Prescha and Karolina Szeremeta
Impact of Vegetarian Diet on Serum Immunoglobulin Levels in Children

Published by:
http://www.sagepublications.com
can be found at: Clinical Pediatrics Additional services and information for

http://cpj.sagepub.com/cgi/alerts Email Alerts:

http://cpj.sagepub.com/subscriptions Subscriptions:
http://www.sagepub.com/journalsReprints.nav Reprints:

http://www.sagepub.com/journalsPermissions.nav Permissions:

What is This?

- Jan 24, 2013 OnlineFirst Version of Record

- Feb 15, 2013 Version of Record >>

at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
Clinical Pediatrics
52(3) 241 246
The Author(s) 2013
Reprints and permission:
sagepub.com/journalsPermissions.nav
DOI: 10.1177/0009922812472250
http://cpj.sagepub.com
Introduction
Nutrition plays an important role in innate, adaptive,
and cellular immune response. The relationship between
nutrition and immunology is bidirectional. First, nutri-
tional status (both malnutrition and overweight) affects
the immune system. On the other hand, immunological
disorders can trigger changes in metabolism and nutri-
tional status.
1
Protein energy malnutrition during child-
hood can arrest immune organ development, and the lack
of appropriate intake of multiple microelements, in par-
ticular zinc, selenium, and iron, can lead to major immu-
nodeficiency and increased susceptibility to infection.
2
Immunoglobulins produced of activated B lympho-
cytes protect the organism against viral and bacterial
infections via neutralization and opsonization of patho-
gens and complement activation. Animal and human
studies show decreased serum immunoglobulin levels
during a low-protein diet.
3-5
There is major interest in studies addressing the
issues of which kinds of diet influence a childs immu-
nity and how. A vegetarian diet is promoted as a healthy
eating model. In general, a well-balanced vegetarian
diet does not adversely affect a childs immunity, but
some authors reported a nutrient deficiency that can
occur as a result of a vegetarian diet.
6,7
In the literature,
there are no data on a vegetarian diets influence on
humoral immune response.
The aim of this study was to assess the serum immu-
noglobulin levels in vegetarian and omnivore children,
and the impact of selected nutrient intake on its level.
Subjects and Methods
Forty children of both sexes, born as full-term infants,
aged 2 to 18 years, were qualified to the study. They
were divided into 2 groups: the group of vegetarian
children (n = 22) and the control group of omnivore
children (n = 18).
The vegetarian subjects were recruited by placing
advertisements in vegetarian magazines and by announce-
ments at the meetings of Hare Krishna believers. The
inclusion criterion of the vegetarian group was that a child
472250CPJXXX10.1177/0009922812
472250Clinical PediatricsGorczyca et al
1
Wroclaw Medical University, Wroclaw, Poland
Corresponding Author:
Daiva Gorczyca, 3rd Department and Clinic of Paediatrics,
Immunology and Rheumatology of Developmental Age, Wroclaw
Medical University, ul. Koszarowa 5, 51-149 Wroclaw, Poland
Email: daiva.gorczyca@am.wroc.pl
Impact of Vegetarian Diet on Serum
Immunoglobulin Levels in Children
Daiva Gorczyca, MD, PhD
1
, Anna Prescha, PhD
1
, and Karolina Szeremeta, MD
1
Abstract
Background. Nutrition plays an important role in immune response. We evaluated the effect of nutrient intake on serum
immunoglobulin levels in vegetarian and omnivore children. Methods. Serum immunoglobulin levels and iron status were
estimated in 22 vegetarian and 18 omnivore children. Seven-day food records were used to assess the diet. Results. There
were no significant differences in serum IgA, IgM, and IgG levels between groups of children. Serum immunoglobulin
levels were lower in vegetarian children with iron deficiency in comparison with those without iron deficiency. In the
vegetarians, IgG level correlated positively with energy, zinc, copper, and vitamin B
6
intake. In the omnivores, these
correlations were stronger with IgM level. Conclusions. Despite negligible differences in serum immunoglobulin levels
between vegetarian and omnivore children, the impact of several nutrient intakes on IgM and IgG levels differed between
groups. Low iron status in vegetarian children can lead to decreased immunoglobulin levels.
Keywords
immunoglobulin, vegetarian diet, children
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
242 Clinical Pediatrics 52(3)
had been following a vegetarian diet for a minimum of
1 year before the examination. The control group consisted
of children without any diseases affecting their growth and
not using any food restrictions. The parents of these chil-
dren volunteered for them to participate in the study.
Our exclusion criteria for both groups were as follows:
current or previous microelement replacement therapy
(within the past 3 months), a diagnosis with recent illness
(shown by a C-reactive protein level greater than 6.0
mg/L), and chronic diseases.
All participants took the questionnaire with Warning
Signs of Immunodeficiency adapted from the International
Union of Immunological Societies Expert Committee.
8
Body weight and height were measured by the same
person using standardized methods and equipment. The
measurements were taken in the morning, before breakfast.
Results of the anthropometric measurements were recorded
on the current Polish growth charts, and then height, weight
were compared with the relevant percentile curves.
The 2.7 mL fasting blood samples were drawn by
venipuncture from each child once early in the morning
between 7 AM and 9 AM. In children from both vegetar-
ian and omnivore groups, the following examinations
were carried out: complete blood count (Beckman Coulter
LH750 counter, Beckman Coulter, Inc, Brea, CA), serum
iron (colorimetric method), total iron-binding capacity
(spectrophotometric method; Ferentest, bioMrieux SA,
Marcy lEtoile, France), serum ferritin (Microparticle
Enzyme Immunoassay; CMIA Architect, Abbott
Laboratories, Abbott Park, IL), and serum immunoglobu-
lin IgG, IgA, and IgM levels (turbidimetry method).
For statistical analysis, anemia was defined as hemo-
globin level <11.0 g/dL, iron deficiency as serum ferri-
tin level <12.0 g/L for children aged 1 to 3 years and
<15.0 g/L for children older than 3 years, and iron defi-
ciency anemia as hemoglobin concentration <11.0 g/dL
with iron deficiency.
9
Dietary intake was assessed using 7-day food records.
The parents were instructed to record all food and bever-
ages consumed at home. The food records were verified by
a trained dietician and analyzed by the computer program
Dieta 4.0 (National Food and Nutrition Institute, Poland).
Statistical analysis was performed using SPSS soft-
ware version 15.0 (SPSS Inc, Chicago, IL). Analyses of
variance with an unpaired Students t test or Mann
Whitney U test and Pearsons correlations or Spearman
rank correlations were performed, depending on the dis-
tribution of variables. P values <.05 were considered to
be statistically significant.
The study protocol was approved by the Ethics
Committee of the University of Medicine in Wroclaw.
Parents (guardians) of the patients and also patients
older than 16 years signed a written consent form before
participating in the study.
Results
As presented in Table 1, the vegetarian group was simi-
lar to the omnivore group in terms of gender, age, body
weight, and height (no significant differences).
None of the participants answered positively for any
of the questions from the primary immunodeficiency
diseases questionnaire. No relevant infectious diseases
were found in the childrens histories in vegetarian and
omnivore groups.
The analysis of hematological parameters and iron
status in the vegetarian and omnivore groups showed
that in the vegetarian group 1 child (4.54%) was diag-
nosed with anemia, 8 children (36.36%) were diagnosed
with iron deficiency, and 2 children (9.09%) were diag-
nosed with iron deficiency anemia. In the omnivore
group, anemia was diagnosed in 1 child (5.55%) and
iron deficiency was diagnosed in 2 children (11.11%).
There were no statistically significant differences in
IgA, IgM, and IgG levels of either group (Table 2). We
found IgA levels under the age limit in 6 (27.27%) chil-
dren, and decreased IgM levels in 2 (9.09%) children in
the vegetarian group. One child (4.55%) in this group
had IgA and IgM deficiency, and 1 child had IgA, IgM,
and IgG deficiency. IgA deficiency was found in 2
(11.11%) children and IgM deficiency in one child
(5.56%) in the omnivore group. Differences in immu-
nodeficiency incidences in both groups were not statis-
tically significant.
The comparison of immunoglobulin levels in vege-
tarian children with iron deficiency and in vegetarian
children without iron deficiency is presented in Table 3.
IgA, IgM, and IgG levels were statistically significantly
lower in vegetarian children with iron deficiency in con-
trast to the vegetarian children without iron deficiency
(P = .021, P = .034, and P = .019, respectively).
The diet analysis (Table 4) showed significantly
higher vitamin C intake in the vegetarian group than in
the omnivore group (69.1 vs 47.3 mg/d; P = .019).
The correlations between serum IgG, IgA, and IgM
levels and selected nutrient intakes, and also selected
hematological parameters in the studied group of chil-
dren are shown in Table 5. We have found that in the
vegetarian group only IgG level correlated positively
with red blood cells, hemoglobin, hematocrit, and ferri-
tin, whereas in the omnivore group, there were no cor-
relations between these parameters. In both groups,
energy, zinc, copper, and vitamin B
6
intake were posi-
tively correlated with IgM levels; however, in the
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
Gorczyca et al 243
omnivore group these correlations were stronger.
Furthermore, a strong positive correlation between IgM
level and protein, fat, iron, and vitamin C (from r =
0.91 to r = 0.95), as well as correlation between energy
intake and IgA level (r = 0.50), was found in the omni-
vore group. In the vegetarian group, a positive correla-
tion between energy, copper, vitamin B
6
, vitamin E,
folic acid intake, and IgG (from r = 0.53 to r = 0.68), as
Table 1. Characteristics of Participants
Characteristics
Vegetarian (n = 22) Omnivores (n = 18)
P n % n %
Age, median (range) 4 years 8 months (1 year to 17 years 7
months)
9 years 5 months (2 years 3 months to
17 years 10 months)
NS
Gender NS
Female 17 77.3 12 66.7
Male 5 22.7 6 33.3
Weight, percentile NS
<25 6 27.3 3 16.7
25-75 10 45.5 8 44.4
>75 6 27.3 7 38.9
Height, percentile NS
<25 5 22.7 2 11.1
25-75 11 50.0 6 33.3
>75 6 27.3 10 55.6
Duration of vegetarian diet, median (range) 3 years 5 months (1 year to 10 years)
Parents are vegetarian and vegetarian diet
started from birth
18 81.8
No vaccinations against childhood diseases 3 13.6
Exposed to tobacco smoke 3 13.6 8 44.4 NS
Angina in anamnesis 2 9.1 NS
Sinusitis in anamnesis 1 4.5 1 5.6 NS
Bronchitis in anamnesis 2 9.1 NS
Urinal tract infections in anamnesis 2 11.2 NS
Iron deficiency anemia (IDA) 2 9.1 NS
Iron deficiency (ID) 8 36.4 2 11.1 .024
Abbreviation: NS, nonsignificant.
Table 2. Serum Immunoglobulin Level in Vegetarian and Omnivore Groups
Vegetarian (n = 22) Omnivores (n = 18) P
IgA (mg/dL); median (range) 116 (0-341) 131 (0-316) NS
IgM (mg/dL); median (range) 129 (29-342) 122 (60-269) NS
IgG (mg/dL); median (range) 998 (387-1734) 954 (727-1353) NS
IgA deficiency; n (%) 6 (27.3) 2 (11.1) NS
IgM deficiency; n (%) 2 (9.1) NS
IgG deficiency; n (%) NS
IgA, M deficiency; n (%) 1 (4.6) 1 (5.7) NS
IgA, IgM, IgG deficiency; n (%) 1 (4.6) NS
Abbreviation: NS, nonsignificant.
Table 3. Serum Immunoglobulin Level in Vegetarian
Children With Iron Deficiency (ID) and With Normal Iron
Status
Vegetarian With ID (n
= 8); Median (Range)
Vegetarian Without ID
(n = 14); Median (Range) P
IgA (mg/dL) 69 (0-189) 149 (0-341) .021
IgM (mg/dL) 90 (29-206) 160 (72-342) .034
IgG (mg/dL) 631 (387-1144) 1073 (587-1734) .0019
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
244 Clinical Pediatrics 52(3)
well as a negative correlation between IgA level and fat
intake was noticed (r = 0.66).
Discussion
To our knowledge, there are no reports on immuno-
globulin levels in children following a vegetarian diet,
so a comparison with other research results is impossi-
ble. In our study, neither differences in infectious dis-
ease morbidity nor significant differences in IgA, IgG,
and IgM serum levels between the vegetarian and omni-
vore groups were observed; however, we analyzed a
relatively small number of subjects and this limits the
generalizablity of our findings.
Table 4. Energy and Selected Nutrition Intake in the Vegetarian and Omnivore Groups
Vegetarian (n = 22) Omnivores (n = 18)
P
Median
(Range)
% RDA
a
; Median
(Range)
Median
(Range)
% RDA
a
; Median
(Range)
Energy (kcal/d) 1255.2 (848.6-1813.7) 84.7
b
(54.6-127.2) 1411.0 (1142.1-1661.5) 87.8
b
(73.6-114.2) NS
Protein (g/d) 22.5 (16.5-46.0) 118.1 (67.6-143.8) 31.6 (13.7-55.5) 112.8 (78.4-148.3) NS
Fat (g/d) 27.8 (18.2-52.7) 51.9 (21.1-91.2) 38.2 (32.9-48.3) 63.2 (45.3-101.5) NS
Linoleic acid (g/d) 3.29 (1.53-6.09) 3.04 (1.97-5.69)
Carbohydrates (g/d) 168.9 (117.6-242.8) 187.6 (173.8-224.8)
Iron (mg/d) 5.99 (3.54-9.19) 66.9 (23.6-115.5) 5.88 (4.41-6.98) 58.6 (37.5-96.9) NS
Zinc (mg/d) 4.02 (1.93-7.15) 75.1 (38.9-197.3) 5.44 (4.68-6.98) 101.7 (67.1-1999.9) NS
Copper (mg/d) 0.66 (0.31-1.28) 163.4 (59.7-383.6) 0.65 (0.60-1.01) 127.5 (68.5-336.8) NS
Vitamin A equivalent (g/d) 1116.1 (771.3-1727.9) 233.6 (73.2-371.3) 594.1 (323.1-2181.2) 126.6 (46.2-483.9) NS
Vitamin B
6
(mg/d) 0.87 (0.50-1.45) 116.1 (49.8-278.6) 1.05 (0.68-1.23) 108.4 (71.5-226.0) NS
Vitamin C (mg/d) 69.1 (44.5-162.33) 171.2 (101.2-405.8) 47.3 (33.5-97.9) 94.7 (51.5-232.8) .019
Tocopherol equivalent (mg/d) 4.57 (1.71-8.51) 71.3
c
(21.4-132.1) 3.64 (2.12-5.18) 52.7
c
(35.4-74.0) NS
Folate (g/d) 132.4 (64.3-237.6) 64.3 (41.2-108.6) 142.8 (122.7-175.3) 58.0 (30.7-116.9) NS
Abbreviations: NS, nonsignificant; RDA, recommended daily allowance.
a
RDA dependent on age and gender.
b
Estimated average requirement (EAR) dependent on age and gender.
c
Adequate intake (AI) dependent on age and gender.
Table 5. Comparison of Immunoglobulin Levels and Selected Nutritional and Hematological Parameters in the 2 Groups
(Correlation Coefficients, r)
a
Parameter
IgA IgM IgG
Vegetarian Omnivores Vegetarian Omnivores Vegetarian Omnivores
Weight 0.41 0.47 0.18 0.23 0.26 0.67
Red blood cells 0.36 0.34 0.38 0.26 0.53 0.20
Hemoglobin 0.49 0.46 0.34 0.31 0.65 0.30
Hematocrit 0.48 0.47 0.44 0.39 0.70 0.24
Serum iron 0.41 0.18 0.04 0.19 0.47 0.47
Ferritin 0.54 0.20 0.45 0.27 0.59 0.42
Total iron-binding capacity 0.10 0.22 0.16 0.35 0.09 0.43
Energy intake 0.45 0.50 0.71 0.96 0.53 0.41
Protein intake 0.15 0.01 0.51 0.95 0.19 0.61
Fat intake 0.66 0.39 0.17 0.90 0.31 0.49
Linoleic acid 0.35 0.14 0.51 0.40 0.48 0.34
Iron intake 0.31 0.29 0.08 0.91 0.12 0.42
Zinc intake 0.34 0.27 0.62 0.95 0.48 0.58
Copper intake 0.46 0.39 0.61 0.98 0.66 0.34
Vitamin A intake 0.11 0.31 0.16 0.98 0.28 0.57
Vitamin B
6
intake 0.56 0.61 0.70 0.95 0.67 0.47
Vitamin C intake 0.28 0.56 0.32 0.93 0.39 0.45
Vitamin E intake 0.46 0.22 0.27 0.03 0.68 0.04
Folic acid intake 0.40 0.25 0.57 0.94 0.62 0.28
a
Statistically significant correlations (P < .05) are given in boldface.
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
Gorczyca et al 245
Protein energy deficiencies had a greater effect on
immune processes. Decreased IgG serum level and thus
increased infection morbidity during a low-protein diet
was demonstrated by Zoppi et al.
3
Furthermore, Kelley
et al
4
showed that energy restrictions lead to decreased
IgG, IgA, C3 levels and a number of circulating natural
killer cells. Differences in neither anthropometric mea-
surements nor energy and protein intake deficiencies
were noticed in the present study, which could explain
the lack of differences in IgG, IgM, and IgA levels in
both groups. In addition, our study showed that energy
and protein intake correlated most highly with IgM
level in the omnivore group. In vegetarians, a signifi-
cant relationship between energy intake and IgM and
IgG was shown.
Vitamin C is a well-known biological antioxidant,
which also affects the activity of natural killer cells, che-
motaxis, and cytokine production.
10,11
Our study dem-
onstrated a greater vitamin C intake in the vegetarian
group in comparison with omnivores. Correlation
between vitamin C intake and IgM serum level was only
observed in the omnivore group. A high vitamin C
intake, exceeding recommendations, could explain the
lack of correlation between these parameters in vegetar-
ian children.
Numerous studies have shown that iron is essential
for cell differentiation and growth, a component of
enzymes critical for the functioning of immune cells.
2

Iron deficiency decreases neutrophil migration by dimin-
ishing the secretion of cytokines (interferon-, tumor
necrosis factor , interleukin-2), which leads to an insuf-
ficiency of intracellular killing of bacteria, and this leads
to an increased susceptibility to infectious diseases. The
effect of iron on humoral immunity is debatable. Some
authors reported no differences in immunoglobulin lev-
els in children with iron deficiency and in healthy chil-
dren.
12
Other publications showed decreased IgA and
IgG levels in children with ID, or subclass IgG4 defi-
ciency, which can lead to recurrent respiratory infec-
tions.
1,13-16
In our study, serum levels of IgA, IgM, and
IgG in vegetarians with iron deficiency were significant
lower than in those with normal hematological parame-
ters; however, this result requires further studies with a
larger group of patients. A strong correlation between
iron intake and IgM level occurring only in the omnivore
group suggests that the differences in iron bioavailability
from vegetarian and omnivore diets could affect the
result.
Zinc intake in Western vegetarians is not critically
low, but often at the lower limit of recommended levels,
and the zinc bioavailability in a vegetarian diet is lower
because of the higher phytic acid content in unrefined
grains, nuts, and legumes.
17,18
Zinc deficiency increases
risk of infection in children.
19
The present study showed
a lower zinc supply in the vegetarian group, in compari-
son with the recommended daily allowance and with
the omnivore group (difference not statistically signifi-
cant). Furthermore, zinc intake correlated with IgM
level in both groups (more strongly in the omnivore
group), which can be attributed to reduced zinc bio-
availability in the vegetarian diet as in the case of iron
intake. The critical limit of zinc intake in the diet has
not been developed yet, thus we cannot draw conclu-
sions on the impact of low zinc intake in the vegetarian
diet. Copper is another microelement closely related to
zinc and it exhibits similar effects in the immune sys-
tem. Because of the lack of appropriate parameters to
determine copper status and the rather efficient homeo-
static regulation of copper status, there are too little
data to reliably evaluate the effect of copper deficiency
or marginal status.
IgM antibodies are predominantly produced by B1
lymphocytes, in the absence of apparent stimulation by
specific antigens, they constitute the major component of
natural antibodies, and they are also the first class of anti-
bodies produced during a primary antibody response.
20
It
is well known that microelement and antioxidant defi-
ciencies quite early lead to changes in the immune sys-
tem.
21
In this study, IgM level seemed to depend on
energy, zinc, copper, and vitamin B
6
intake in both veg-
etarian and omnivore children, whereas IgG level corre-
lated significantly with copper, vitamin B
6
, vitamin E,
and folate intake only in vegetarians.
Conclusions
In this study, we found no differences in IgG, IgM, IgA
levels between vegetarian and omnivore groups. Low
iron status affected IgG level in the vegetarian group.
IgM level correlated positively with zinc, copper, and
vitamin B
6
intake in both groups, although the correla-
tion was stronger in the omnivore group.
Acknowledgments
We gratefully acknowledge all participating children and their
parents for their collaborations.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
Funding
The author(s) disclosed receipt of the following financial sup-
port for the research, authorship, and/or publication of this
article:
This work was supported by the Wroclaw Medical
University (Grant No. 1037/2006).
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from
246 Clinical Pediatrics 52(3)
References
1. Cunningham-Rundles S, McNeeley DF, Moon A. Mecha-
nisms of nutrient modulation of the immune response. J
Allergy Clin Immunol. 2005;115:1119-1128.
2. Wintergerst ES, Maggini S, Hornig DH. Contribution of
selected vitamins and trace elements to immune function.
Ann Nutr Metab. 2007;51:301-323.
3. Zoppi G, Zamboni G, Siviero M, Bellini P, Cancellieri
ML. Gamma-globulin level and diet protein intake during
the first year of life. Pediatrics. 1978;62:1010-1018.
4. Kelley DS, Daudu PA, Branch LB, Johnson HL,
Taylor PC, Mackey B. Energy restriction decreases num-
ber of circulating natural killer cells and serum levels of
immunoglobulins in overweight women. Eur J Clin Nutr.
1994;48:9-18.
5. Amaral JF, Foschetti DA, Assis FA, Menezes JS, Vaz
NM, Faria AM. Immunoglobulin production is impaired
in protein-deprived mice and can be restored by
dietary protein supplementation. Braz J Med Biol Res.
2006;39:1581-1586.
6. Sanders TA, Reddy S. Vegetarian diets and children. Am
J Clin Nutr. 1994;59:1176-1181.
7. Kirby M, Danner E. Nutritional deficiencies in children
on restricted diets. Pediatr Clin North Am. 2009;56:1085-
1103.
8. Notarangelo LD, Fischer A, Geha RS, et al; Inter-
national Union of Immunological Societies Expert
Committee on Primary Immunodeficiencies. Primary
immunodeficiencies: 2009 update. J Allergy Clin Immu-
nol. 2009;124:1161-1178.
9. World Health Organization. Assessing the iron status of
populations. Geneva, Switzerland: World Health Orga-
nization; 2007: 49-55. http://apps.who.int/iris/bitstr
eam/10665/75368/1/9789241596107_eng.pdf
10. Jeng KC, Yang CS, Siu WY, Tsai YS, Liao WJ, Kuo JS.
Supplementation with vitamin C and E enhances cyto-
kine production by peripheral blood mononuclear cells in
healthy adults. Am J Clin Nutr. 1996;64:960-965.
11. Wintergerst ES, Maggini S, Hornig DH. Immune-
enhancing role of vitamin C and zinc and effect on clini-
cal conditions. Ann Nutr Metab. 2006;50:85-94.
12. Bagchi K, Mohanram M, Reddy V. Humoral immune
response in children with iron-deficiency anaemia. BMJ.
1980;280:1249-1251.
13. Chandra RK, Saraya AK. Impaired immunocompetence
associated with iron deficiency. J Pediatr. 1975;86:
899-902.
14. Guzikowska E, Cholewa Z, Bujniewic E, Moskaa
H, Guzikowski K, Madeyski J. Various parameters of
humoral and cellular immunity in children with iron defi-
ciency [in Polish]. Pol Tyg Lek. 1989;44:718-719.
15. Feng XB, Yang XQ, Shen J. Influence of iron deficiency
on serum IgG subclass and pneumococcal polysac-
charides specific IgG subclass antibodies. Chin Med J.
1994;107:813-816.
16. Ekiz C, Agaoglu L, Karakas Z, Gurel N, Yalcin I. The
effect of iron deficiency anemia on the function of the
immune system. Hematol J. 2005;5:579-583.
17. Craig WJ. Nutrition concerns and health effects of veg-
etarian diets. Nutr Clin Pract. 2010;25:613-620.
18. Thane CW, Bates CJ. Dietary intakes and nutrient status
of vegetarian preschool children from a British national
survey. J Hum Nutr Diet. 2000;13:149-162.
19. Walker CL, Black RE. Zinc treatment for serious infec-
tions in young infants. Lancet. 2012;379:2031-2033.
20. Boes M. Role of natural and immune IgM antibodies in
immune responses. Mol Immunol. 2000;37:1141-1149.
21. Chandra RK. Nutrition and the immune system: an intro-
duction. Am J Clin Nutr. 1997;66:460S-463S.
at Yale University Library on March 22, 2013 cpj.sagepub.com Downloaded from