(Chest. 2000;118:1150-1157.)
© 2000
American College of Chest Physicians
Chicken Soup Inhibits Neutrophil Chemotaxis In Vitro*
Barbara O. Rennard, BA;
Ronald F. Ertl, BS;
Gail L. Gossman, BS;
Richard A. Robbins, MD, FCCP and
Stephen I. Rennard, MD, FCCP
*
From the Pulmonary and Critical Care Medicine Section, Nebraska Medical Center, Omaha, NE.
Correspondence to: Stephen I. Rennard, MD, FCCP, Larson Professor of Medicine, Pulmonary and Critical Care Medicine Section, 985125 Nebraska Medical Center, Omaha, NE 68198-5125; e-mail: srennard{at}unmc.edu
 |
Abstract
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Chicken soup has long been regarded as a remedy for
symptomatic upper respiratory tract infections. As it is likely that
the clinical similarity of the diverse infectious processes that can
result in "colds" is due to a shared inflammatory response, an
effect of chicken soup in mitigating inflammation could account for its
attested benefits. To evaluate this, a traditional chicken soup was
tested for its ability to inhibit neutrophil migration using the
standard Boyden blindwell chemotaxis chamber assay with
zymosan-activated serum and fMet-Leu-Phe as chemoattractants. Chicken
soup significantly inhibited neutrophil migration and did so in a
concentration-dependent manner. The activity was present in a
nonparticulate component of the chicken soup. All of the vegetables
present in the soup and the chicken individually had inhibitory
activity, although only the chicken lacked cytotoxic activity.
Interestingly, the complete soup also lacked cytotoxic activity.
Commercial soups varied greatly in their inhibitory activity. The
present study, therefore, suggests that chicken soup may contain a
number of substances with beneficial medicinal activity. A mild
anti-inflammatory effect could be one mechanism by which the soup could
result in the mitigation of symptomatic upper respiratory tract
infections.
Key Words: chicken soup • neutrophil chemotaxis
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Introduction
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Chicken
soup has been regarded as a remedy for centuries. The Egyptian Jewish
physician and philosopher Moshe ben Maimon (Maimonides) recommended
chicken soup for respiratory tract symptoms in his 12th century
treatise, reportedly drawing on classical Greek
sources.1
2
3
4
So widely recommended is chicken soup in the
Jewish tradition, that it is referred to by a variety of synonyms as
Jewish penicillin, bohbymycetin, and bobamycin.5
6
Chicken
soup is, however, also recommended for similar purposes in a variety of
other traditions suggesting multiple independent
discoveries.7
Colds are generally the result of transient infections of the mucosa of
the upper respiratory tract with a variety of viruses including, but
not limited to, the rhinoviruses.8
9
10
While incompletely
understood, the viral infection leads to the stimulation of
acytokine cascade.11
12
It is likely that many, if not
most, of the symptoms related to colds are consequent to the
inflammatory response thus initiated.13
14
15
The activation
of common physiologic pathways likely accounts for the marked
similarity of symptoms that result from colds. In this regard, colds
are associated with the generation of neutrophil chemotactic
activities11
12
13
15
and with the recruitment of
neutrophils to the epithelial surface of the
airways.12
13
16
17
Since neutrophil products are potent
secretagogues,18
this may be one mechanism by which colds
commonly lead to cough and sputum from a diverse set of infections.
Chicken soup may have a number of beneficial effects for an individual
with a cold. These could include actions as diverse as improving
hydration and nutritional status19
and accelerating
mucosal clearance.5
The nature of the direct cytotoxic
actions on microorganisms are controversial.6
20
21
Another potential mechanism for beneficial effects could be an
attenuation of the inflammatory response. In order to evaluate that
possibility, the ability of chicken soup to inhibit neutrophil
chemotaxis in response to standard chemotactic stimuli was evaluated
and demonstrated in the current study. These results provide one
mechanistic basis in support of the traditional claims made for chicken
soup as a remedy.
|
Materials and Methods
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Soup
Traditional chicken soup was prepared according to a
family recipe, which will be referred to as "Grandma’s
soup" (C. Fleischer; personal communication; 1970).
This recipe is as follows:
• 1 5- to 6-lb stewing hen or baking chicken;
• 1 package of chicken wings;
• 3 large onions;
• 1 large sweet potato;
• 3 parsnips;
• 2 turnips;
• 11 to 12 large carrots;
• 5 to 6 celery stems;
• 1 bunch of parsley; and
• salt and pepper to taste.
Clean the chicken, put it in a large pot, and cover it
with cold water. Bring the water to a boil. Add the chicken wings,
onions, sweet potato, parsnips, turnips, and carrots. Boil about
1.5 h. Remove fat from the surface as it accumulates. Add the
parsley and celery. Cook the mixture about 45 min longer. Remove the
chicken. The chicken is not used further for the soup. (The meat makes
excellent chicken parmesan.) Put the vegetables in a food processor
until they are chopped fine or pass through a strainer. Both were
performed in the present study. Salt and pepper to taste. (Note: this
soup freezes well.) Matzoh balls were prepared according to the recipe
on the back of the box of matzoh meal (Manischewitz; Jersey City,
NJ).
Three separate preparations of soup were made. The completed soup was
collected from all three. In addition, in order to determine at which
stage the soup acquired activity, 19 samples were collected during the
preparation of one batch (Table 1
). As the mixture was inhomogeneous, several samples were collected at
the same time from different regions of the pot. All samples were
frozen in small aliquots and stored (-80°C) until assay.
In order to determine whether particulates accounted for the activity
of the soup, attempts were made to obtain a clarified preparation. Soup
that was prepared by this method could not be passed through a
0.22-µm filter. In order to remove particulates, 1-mL aliquots were
centrifuged (12,000g for 15 min) in Eppendorf tubes.
This resulted in a visible pellet and a clarified transparent yellow
supernatant, which was aspirated for subsequent assay.
To determine which components of the soup contained inhibitor activity,
samples of chicken (a leg) and a portion of each of the vegetables were
boiled for approximately 1 h. The supernatant broths then were
harvested, frozen, and saved for assay.
For comparison purposes, commercially available soups were obtained
from a local supermarket and prepared according to the directions on
the packaging. No strict quality control was performed, although each
preparation was evaluated by taste and was felt to be satisfactory (if
variably so).
Neutrophil Chemotaxis
Peripheral blood was collected from healthy nonsmoking
volunteers under a protocol approved by the University of Nebraska
Institutional Review Board and by sedimentation through dextran, as
described previously.22
Neutrophils then were rinsed,
suspended at 106 cells/mL in Hank’s balanced
salt solution (HBSS), and used as targets for chemotaxis. Chemotaxis
was performed by the modified blindwell technique using 48-well
multichambers and 3-µm pore size polycarbonate filters (Nucleoprobe;
Cabin John, MD), as described previously.23
Soup Inhibition of Neutrophil Chemotaxis
In order to determine whether the soup could inhibit chemotaxis,
dilutions of soup (1:100) were added to the top and bottom wells of the
chemotaxis chamber. Zymosan-activated serum (ZAS)24
was
used as the positive chemoattractant. As a control to determine whether
chicken soup had chemotactic activity, chicken soup was added directly
to the bottom of the chemotaxis chamber without other chemoattractants.
Concentration Dependence of Chicken Soup Effect
Serial dilutions of chicken soup were added to neutrophils in
the upper portion of the chemotaxis chamber, and ZAS (1:4) or
fMet-Leu-Phe (fMLP), 10-7 mol/L (Sigma; St.
Louis, MO), were used as chemoattractants.
Viability
In order to determine whether soup and its components were
cytotoxic, neutrophils were prepared as if for chemotaxis and were
suspended in HBSS with a 1:100 dilution of soup, component vegetables,
or chicken extracts. After a 30-min incubation at 37°C, cells were
collected and viability was assessed by trypan blue dye exclusion
visually.
Statistics
For data sets with multiple comparisons, analysis of variance
was first used to determine whether any group was significantly
different, following which Student’s t test was used for
comparisons that appeared to be different. Data presented are mean
± SEM.
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Results
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Chicken soup was found to inhibit neutrophil chemotaxis. When the
completed soup (without added salt and pepper) was added to neutrophils
above the membrane, to the ZAS below the membrane, or to both sides of
the chemotaxis membrane, neutrophil migration to ZAS was inhibited. The
effect of the chicken soup was much more marked when the diluted
chicken soup was added directly to the neutrophils (Fig 1
). The diluted chicken soup by itself had a minimal effect in
stimulating neutrophil chemotaxis above background in the absence of a
chemoattractant (Fig 1)
.
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Figure 1. Inhibition of neutrophil chemotaxis by chicken
soup. ZAS (dilution, 1:4) and chicken soup (cs) (prep 1, fraction 18
diluted 1:100) were added to the top and bottom of the chemotaxis
chamber in various combinations as indicated. Neutrophils were added to
the top of the chamber, and neutrophil chemotaxis performed. Vertical
axis: migrated neutrophils (cells per high-power field [hpf]).
Horizontal axis: condition. * = p < 0.05.
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The inhibitory effect of chicken soup was concentration-dependent and
was observed when both ZAS and fMLP were used as chemoattractants (Fig 2
). Interestingly, chicken soup added to the neutrophils at dilutions of
> 1:20 caused a slight but significant (p < 0.05) increase in
neutrophil migration toward media controls (Fig 2)
. Three
preparations of chicken soup inhibited chemotaxis to ZAS similarly (Fig 3
). It was not possible to remove the particulate matter from the chicken
soup by filtration. In order to determine whether the solid component
of the chicken soup might be responsible for the inhibition of
chemotaxis, therefore, the chicken soup was clarified by centrifugation
at high speed. Although there was some loss of activity, the clarified
supernatants of the three chicken soup preparations retained the
majority of inhibitory activity (Fig 3)
.
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Figure 2. Inhibition of neutrophil chemotaxis and
concentration dependence. Chicken soup (preparation No. 1, fraction No.
18) was placed in varying dilutions together with neutrophils in the
upper portion of the chemotaxis chamber. ZAS, fMLP, or Dulbecco’s
modified Eagle’s medium (DMEM) was placed in the lower portion of the
chemotaxis chamber as a chemoattractant. Chemotaxis then was performed.
* = p < 0.05 compared to the highest dilution.
HPF = high-power field.
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Figure 3. Inhibition of chemotaxis by various preparations
and the effect of clarification. Three separate preparations of chicken
soup were tested either in the completed stage (solid bars) or after
clarification by centrifugation (15 min, 12,000g,
stipple bars). All samples were diluted 1:40 into HBSS and were added
together with the neutrophils. ZAS, diluted 1:4, was used as the
chemoattractant. HBSS and ZAS alone are shown as negative and positive
controls, respectively. Vertical axis: migrated neutrophils. Horizontal
axis: conditions. * = p < 0.05 compared to ZAS control. See
Figure 2
for other abbreviations.
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In an attempt to partially determine which components of chicken soup
had activity, two experimental approaches were undertaken. First,
samples of chicken soup were harvested at various times during the
preparation. As the soup preparation was exceedingly inhomogeneous,
samples were taken from various parts of the pot at various times.
Samples containing the initial stages of the soup with early chicken
broth alone were not active (Fig 4 ). All samples harvested after the addition of the first group of
vegetables had inhibitory activity. In the final stages of the
preparation, slightly less inhibition of chemotaxis was observed.
Second, an analysis of individual soup components was performed by
boiling individual components. All ingredients were found to be
inhibitory, including the boiled extract of chicken alone (Fig 5
, top). The effect on the inhibition of the whole soup was
not due to effects on neutrophil viability. The viability of
neutrophils exposed to each of the complete chicken soup preparations
was always > 95%. The viability of the neutrophils incubated in the
boiled chicken stock was 98%. The isolated vegetable components,
interestingly, demonstrated a slight, but statistically significant,
loss of neutrophil viability, as assessed by trypan blue exclusion (Fig 5
, bottom).
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Figure 4. Acquisition of chemotactic inhibitory activity
during preparation of the soup. Samples were collected at various
stages during the preparation of chicken soup. Each aliquot then was
diluted 1:100 into HBSS and was added together with neutrophils in the
top portion of the chemotaxis chamber. Chemotaxis then was measured
using ZAS diluted 1:4 as the chemoattractant. The major stages of the
soup preparation are indicated. See Figure 2
for other abbreviations.
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Figure 5. The effect of specific vegetable ingredients on
the inhibition of chemotaxis and neutrophil viability.
Top: the component ingredients of chicken soup were
boiled in water after which they were sonicated, diluted 1:100 in HBSS,
and added to neutrophils in the top portion of a chemotaxis chamber.
ZAS diluted 1:4 was used as the chemoattractant. Bottom:
viability was assessed by trypan blue dye exclusion after incubating
the neutrophils in HBSS with the diluted soup components for 30 min.
See Figure 2
for other abbreviations.
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In a modest attempt to determine whether commercially available
preparations of chicken soup also inhibited neutrophil chemotaxis, 13
different soups were purchased at a local supermarket and were tested
against Grandma’s soup (Fig 6)
. Many of the soups inhibited neutrophil
chemotaxis. Five inhibited more potently (at an identical dilution)
than did Grandma’s traditional soup. Two soups were without activity,
and one slightly augmented chemotaxis. Omaha tap water had no activity.
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Figure 6. The effect of various commercial soups on
neutrophil chemotaxis. A number of preparations of soup were purchased
at a local supermarket and were prepared according to the instructions
on the label. All samples then were diluted 1:40 in HBSS added to
neutrophils, and chemotaxis to ZAS (diluted 1:4) was tested. See Figure 2
for other abbreviations.
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Discussion
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The current study demonstrates that chicken soup inhibits
neutrophil migration to standard stimuli as assessed by the modified
Boyden blindwell chamber method. The effect appears to be due to an
effect on the neutrophils rather than on the chemoattractant, as
addition of the soup directly to the neutrophils appears to be most
effective. The inhibitory effect was observed clearly at concentrations
without cytotoxicity, as determined by trypan blue dye exclusion.
Finally, a variety of soup preparations was evaluated and found to be
variably, but generally, able to inhibit neutrophil chemotaxis. The
current study, therefore, presents evidence that chicken soup might
have an anti-inflammatory activity, namely, the inhibition of
neutrophil migration.
The identity of the active ingredient or ingredients present in the
soup remains unknown. The vegetables that are used to prepare the soup,
however, are known to contain a large number of chemical species, many
of which have medicinal activities.25
26
27
A number of fats
and substances with antioxidant activity are also likely to be present.
Extracts of each vegetable, as well as of the chicken, all were able to
inhibit neutrophil chemotaxis, suggesting that many inhibitory
substances may be present. Interestingly, the vegetable extracts also
demonstrated some neutrophil cytotoxicity that was not observed either
in the completed soup or in the chicken extract. No attempt was made to
control for concentration of various extracted components, and the
toxicity could be due to a concentration-dependent effect. However, the
preparation of the soup is a multistep process, and many complex
chemical interactions are taking place. Determining these processes
quantitatively and preparing appropriately controlled component
extracts will be a challenging problem.
It is interesting, however, that neither the chicken nor the completed
soup had cytotoxicity. There are several possibilities in addition to
concentration effects that could explain such an effect. The chicken
may contain a component that chemically neutralizes vegetable-derived
toxins. Alternatively, the fat that is slowly extracted from the
chicken and then skimmed from the soup surface could be extracting a
lipid-soluble toxin from the preparation. That some interaction takes
place during the cooking seems likely as the soup acquires maximal
inhibitory activity shortly after adding the first group of vegetables.
While still active, inhibitory activity does decrease slightly during
the later stages of the preparation. Finally, it also is possible that
the chicken could contain a component that directly activates
neutrophils and has a protective effect, eg, by inducing
antioxidants.
The current study assessed a single measure of the inflammatory
response, migration of neutrophils by the blindwell assay method.
Chicken soup inhibited chemotaxis to two different chemoattractants,
ZAS, which generates the active fragment of the fifth component of
complement, C5a,24
and fMLP.28
In vivo inflammatory responses are complex and multifaceted.
Whether chicken soup has other activities remains to be determined. It
was of interest, however, that while able to inhibit
chemoattractant-driven migration, the soup had a slight direct
chemotactic activity and may have slightly augmented nondirected
migration. These effects, while statistically significant, were small
and were not pursued in the current study. However, their presence
suggests that chicken soup contains a multitude of moieties with
diverse physiologic effects.
The chicken soup recipe used for the majority of these experiments is
very highly regarded locally.29
It does have several
unusual features, however. First, it contains several vegetables,
eg, sweet potato, not found in many chicken soup recipes; in
addition, in many recipes, the vegetables are removed from the clear
broth prior to serving. After removal, Grandma’s soup calls for the
vegetables to be pureed and added to the soup. (We understand that this
was a modification introduced by Grandma during the Great Depression to
ensure that everyone ate the available vegetables.) The soup, as a
result, contains a thick suspension of particulates.
Particulates can interact with neutrophils and could, perhaps,
interfere with chemotaxis.30
However, for several reasons,
it seems unlikely that particulates account for the majority of the
activity. First, Grandma’s soup, clarified by centrifugation, retained
the majority of inhibitory activity. Second, Grandma’s soup
preparation was active prior to the addition of the pureed vegetables,
the major source of particulates. Finally, inhibitory activity was
observed with several other recipes that lack the vegetable
particulates. Thus, while the identity of the biologically active
materials is unknown, it seems likely they are water soluble or
extractable.
Whether the active moieties present in chicken soup achieve sufficient
concentration to be active following in vivo ingestion is
not known. The identity of these moieties is not known, and
bioavailability testing was beyond the scope of the current study. The
activity is water extractable, however, suggesting that it may be
absorbable. The inhibitory effect of chicken soup on neutrophil
chemotaxis, moreover, was observed at dilutions as low as 1:200. This
is comparable to the dilution of a 350-mL "average" bowl of soup
eaten by a 70-kg person. The observations that activities are present
in the clarified soup, are active at a dilution that was comparable to
that of one bowl diluted into a body volume, and are water extractable
are consistent, when taken together, with a potential in
vivo effect.
Undoubtedly, the in vivo effects of chicken soup include
more than the effects on neutrophils. The warm liquid, particularly
when sipped, can stimulate nasal clearance and may improve upper
respiratory tract symptoms.5
The social setting in which
chicken soup is often taken is likely to contribute to a strong placebo
effect. Despite the observation that neutrophil chemotactic inhibitors
are present in many vegetable extracts, pureed carrots (or other
vegetables) are not recommended as a remedy, while chicken soup is.
This suggests that whole chicken soup may contain a mixture of active
agents that synergize each other in order to achieve their beneficial
effects. It is also consistent with the recommendation that the use of
chickens of a certain age1
that are, perhaps,
happy31
is more effective. Such a synergism would
not be surprising, as it is certainly true for taste (this observation
is from common knowledge and general experience).
Chicken soup is not without hazard. Anaphylaxis,28
aspiration,32
33
34
and severe electrolyte
disturbances36
37
all have been described as a result of
chicken soup ingestion. An anti-inflammatory effect could increase the
risk for secondary infection. The benefits of chicken soup, however,
are widely acclaimed and have been the subject of several
reviews,1
7
although the anecdotal nature of the clinical
evidence supporting a benefit of chicken soup is well
recognized.20
21
These benefits range from alleviation of
symptoms of respiratory tract infection,1
2
3
5
6
7
to
possibly improving aircraft fuel usage,37
although the
data supporting some of these various claims are meager, and many of
these reports lack scientific vigor. The current study was well
controlled and used well-established in vitro methods to
provide limited evidence that chicken soup could have an
anti-inflammatory activity. Since many of the symptoms that follow
upper respiratory tract viral infections may well be due to the
inflammatory response, the current study may have clinical relevance.
Prolonged benefits of chicken soup also have been reported in some
settings.38
It has been suggested that even transient
respiratory tract inflammation can cause prolonged worsening of
asthma.39
Should chicken soup reduce respiratory tract
inflammation in vivo, there may be a prolonged benefit. It
is more difficult, however, to relate the results of the present study
to some of the other claims made for chicken soup, but the authors have
no doubt that such speculations have been made in good taste.
The current study demonstrates a statistically significant inhibition
of neutrophil chemotaxis by chicken soup in vitro. This was
not an in vivo clinical trial. Whether clinical benefits
would be obtained with the chicken soup used in the current study or
not, therefore, remains untested. Many readers of this journal will
have had personal experience with the ingestion of chicken soup in the
setting of respiratory tract symptoms or other illnesses. Many
clinically efficacious therapies have been discovered through careful
observation. The present study provides one piece of evidence that
chicken soup contains compounds of potential medical value. No doubt,
many other traditional remedies do as well. The evaluation of
traditional remedies by rigorous modern methods has the potential to
expand our therapeutic armamentarium.
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Acknowledgements
|
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The authors thank Ms. Lillian Richards for
both general and secretarial support, Drs. Gerald Baum, Irving Zucker,
and Irwin Ziment for their useful discussions. (The recipe for Dr.
Ziment’s chicken soup, a formula developed from Ms. Yda Ziment, which
he finds of great value in vivo, is available
elsewhere.40
It was not tested as a comparator here, there
being a limit to tests to which Grandma’s soup recipe should be
subject.) We also thank Mrs. Doris Oglander for consultations regarding
Grandma’s soup recipe and Rachael, Emily, Sarah, Hannah, David,
Rebecca, Naomi, and Dena Rennard for assistance in quality control.
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Footnotes
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Abbreviations: fMLP = fMet-Leu-Phe;
HBSS = Hank’s balanced salt solution; ZAS = zymosan-activated
serum
Received for publication November 17, 1998.
Accepted for publication April 3, 2000.
|
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Abstract
Introduction
