International Journal of Pediatric Otorhinolaryngology (2003) 67, 365
/371

www.elsevier.com/locate/ijporl

Dysfunction of peripheral blood granulocyte

oxidative metabolism in children with recurrent
upper respiratory tract infections
Malgorzata Kowalskaa,*, Halina Kowalskaa, Lidia Zawadzka-Glosb,
c, Mieczyslaw Chmielikb, Maria Wa
Malgorzata De
bskab, Ewa Szerszen
sika
a

Department of Laboratory Diagnostics and Clinical Immunology of Developmental Age, Warsaw

University School of Medicine, Warsaw, Poland
b
Department of Paediatric Otolaryngology, Warsaw University School of Medicine, Warsaw, Poland
c
Paediatric Outpatient Department, Warsaw, Poland
Received 11 April 2002; received in revised form 27 November 2002; accepted 1 December 2002

KEYWORDS
Recurrent upper respiratory tract infections;
Tonsillar hypertrophy;
Granulocyte chemiluminescence

Summary Granulocytes play a key role in the defence against bacterial infections.
Their dysfunction may both predispose to and result from infections. The oxidative
metabolism of peripheral blood granulocytes was studied in 50 children aged from 1
to 10 years, with recurrent upper respiratory tract infections and/or tonsillar
hypertrophy. Four groups of patients were recruited: 15 healthy controls, seven
patients with idiopathic tonsillar hypertrophy, 12 patients with upper respiratory tract
infections and 16 patients with upper respiratory tract infections with concurrent
tonsillar hypertrophy. The ability of granulocytes to produce reactive oxygen species
was assessed by nFMLP-induced chemiluminescence. Both increased and depressed
granulocyte activity was observed in all studied groups, with the exception of
controls. Altered granulocyte function was observed in 30% of patients in the
idiopathic tonsillar hypertrophy group. In children with recurrent infections abnormal
chemiluminescence results were found in from 75% to nearly 90% of patients. This
preliminary study demonstrates the possible relationship between recurrent upper
respiratory tract infections, tonsillar hypertrophy and impaired peripheral blood
granulocyte chemiluminescence.
2003 Elsevier Science Ireland Ltd. All rights reserved.

1. Introduction
Upper respiratory tract infections are among the
most common problems encountered in paediatric
practice [1,2]. Mild and rapidly reducing infections
do not arouse concern; those that recur despite

*Corresponding author.
E-mail address: wasik@litewska.edu.pl (M. Kowalska).

treatment pose problems. Recurrent infections of

the mouth, pharynx, nose and ears may be the
earliest signs of immunodeficiency. In a report from
the LeBonheur Childrens Medical Center, in 14 of
18 retrospectively studied patients with a diagnosis
of inborn SCID (Severe Combined Immunodeficiency Syndrome) the disease manifested itself as
recurrent upper respiratory tract infection [3].
Many children with recurrent upper respiratory

0165-5876/03/$ - see front matter 2003 Elsevier Science Ireland Ltd. All rights reserved.
doi:10.1016/S0165-5876(02)00402-0

366

tract infections develop hypertrophy of the throat

lymphatic tissue. Several studies demonstrated the
role of bacterial tissue colonisation in the pathogenesis of adenoidal and tonsillar hypertrophy
[4,5]. Obturation of the airways, and otitis media
with effusion lead to adenotonsillectomy or adenotomy in these patients [6]. Impaired tonsilllar
and adenoidal lymphocytes proliferative response
to non-typeable Haemophilus influensae antigen,
and decreased local production of IgA and IgG was
observed in children with hypertrophy of the
pharyngeal lymphatic tissue and concurrent otitis
media [7,8]. In some operated patients, lack of a
history of recurrent infections suggests that the
hypertrophy is idiopathic. In our previous reports
on patients qualified for adenotosillotomy we have
described the qualitative and quantitative disorders of lymphocyte subpopulations of peripheral
blood and tonsils [9,10].
In the light of current knowledge about the
complexity of the immune system, it seems justified to include the widest possible laboratory test
panels evaluating both specific and non-specific
immunity and factors regulating their activity in
examination of children with recurrent upper
respiratory tract infections. There are few such
reports in either the immunological or otorhynolaryngological literature. As a continuation of our
work on changes in the immune system of children
with tonsillar hypertrophy, we looked at the
tendency towards recurrent upper respiratory tract
infections in this group, and compared it with that
found in children without throat lymphatic tissue
hypertrophy. In this study we describe the peripheral granulocyte activity in the investigated children, determined by the measurement of
spontaneous and induced light emission.

2. Material and methods

Fifty children aged from 1 to 10 years, 26 boys
and 24 girls, with recurrent upper respiratory tract
infections and/or tonsillar hypertrophy, were enrolled in the study. Patients with recurrent upper
respiratory tract infections had at least eight
episodes of sore throat and fever per year. The
size of the tonsils was evaluated according to the
classification given by Cotton and Myer [11],
comparing the distance between the anterior
pillars with the space occupied by the tonsils.
Pharyngeal lymphatic tissue size was defined in a
following way: tonsils in fossa */size 0 and tonsils
occupying 25, 50, 75% and more than 75% of the
oropharyngeal way reflected size /1, /2, /3 and
/4, respectively.

M. Kowalska et al.

Based on disease history and physical examination, the children were divided into the following
groups:
1) Controls (C; n/15) */healthy children with
negative history of recurrent upper respiratory
tract infections and tonsils size 0, /1.
2) Children with idiopathic tonsillar hypertrophy
(T; n /7) */patients qualified for adenotonsillotomy due to important airway obstruction
(tonsils size /3, /4) with negative history of
recurrent upper respiratory tract infections.
3) Children with recurrent upper respiratory tract
infections without tonsillar hypertrophy (I; n /
12) */patient with tonsils size 0, /1 and
positive history of recurrent upper respiratory
tract infections.
4) Children with recurrent upper respiratory tract
infections and concurrent tonsillar hypertrophy
(TI; n /16) */patient with tonsils size /2, /
3, /4 admitted to the hospital for adenotonsillectomy, with positive history of recurrent
upper respiratory tract infections.
The age and sex distribution was similar in all
groups. The children in the control group were
healthy pupils of nursery and a sports-oriented
primary school. The children in the studied groups
had no other diseases except those on the basis of
which they were qualified for the above groups.
During the study, all of the children had no signs
of infection and the results of carried out basic
laboratory tests (blood count and smear, erythrocyte sedimentation rate, urinalysis) were all within
the normal range. None of the children received
any medications and the time from their last
infection, antibiotictherapy and vaccination was
at least 4 weeks before material was sampled for
the study.
Two millimetres of blood were taken from the
ulnar vein to a tube containing heparin (10 u/ml).
The blood count was determined using a Coulter
Micro Diff II analyser, nucleated blood cells being
identified microscopically after haematological
staining. Urinalysis was conducted using a Clinitec
100 (Bayer) analyser. Erythrocyte sedimentation
rate was determined using an automatic instrument, Monitor 20E (Oxford).
The chemiluminescence test based on measuring
the light emitted spontaneously and after stimulation was performed in the presence of luminol in a
Wallac 1409 scintillation counter (Wallac, Finland).
Chemiluminescence was measured in every blood
sample, before and after stimulation, with nFMLP
peptide, prepared at a concentration of 10 5 M.
Samples and reagents were prepared as described

Dysfunction of peripheral blood granulocyte oxidative metabolism in children

earlier [12]. The recorded light impulses (in 10 ml

blood) were expressed per granulocytes (g) per ml
of blood (imp/g). The stimulation index was
calculated using the formula: (st/sp)/sp, where
sp is the number of spontaneous light impulses
(mean value from 10 measurements taken every 15
s), and st, the number of stimulated impulses at
peak response.
Bacteriological study was performed in patients
with tonsillar hypertrophy undergoing elective
adenotosillotomy (TI and T groups). Two swabs
were taken: one from the surface of the tonsil */
before the operation, second from the core of the
tonsil, resected during the surgery. Removed tonsil
were placed in a sterile 0.9% NaCl solution,
washed, cut with a sterile scalpel and the swab
was taken from the core of the tonsil. The swabs
were cultivated on the following mediums: Columbia CN blood agar, McConkey agar, non-selective
enriched chocolate agar; incubation aerobic and
uder 5% carbon dioxide. Bacteria were identified
using the serological Bio Merieux tests (Slidex
Strepto Kit ABCDEFG, Slidex Pneumo Kit, Slidex
Staph Kit, API NH, ID32GN and optochin test).
Statistical analysis was conducted using Statistica software, non-parametric Mann
/Whitney test,
Wilcoxons and x2-tests. A probability of less than
or equal to 0.05 was considered significant.
Parents of the investigated children, gave their
written consent, having been fully informed of the
nature, risks and the potential benefits of the
study. In cases of elder children we also obtained
their permission for the examination. The research
and the ethical committee of Warsaw University
School of Medicine approved the investigation.

3. Results
The average leukocyte counts, absolute number
of granulocytes and their percentages are given in
Table 1. Both the leukocyte count and number of

367

granulocytes in the groups of sick children did not

differ from values found in healthy controls.
Patients individual results of spontaneous and
stimulated chemiluminescence and the calculated
indexes are presented in Table 2. Additionally, the
comparison the mean chemiluminescence values in
the investigated groups is given in Table 3. In all of
the studied groups of children, with the exception
of controls, the results of both spontaneous and
stimulated chemiluminescence were highly dispersed. In all three studied groups, the average
number of spontaneous emissions of light per
granulocyte was several times higher than in
controls, but were only significant in (I) group
(Table 3). The average number of light impulses per
cell after stimulation with nFMLP was also several
times higher in the group of sick children than in
controls. A significant rise in comparison with
controls was observed in groups (I) and (TI).
In the control group, chemiluminescence induced by nFMLP was always at least three times
higher than of spontaneous chemiluminescence.
The lowest index was 3.14, the highest 12.94,
average 5.749/2.77 (Table 2). In the groups of
studied children, however, a very wide range of
individual responses was observed, and a high
spontaneous result was not always accompanied
by an equally high response to the stimulus. On the
basis of the control group results it was assumed
arbitrarily that the lack of at least a twofold
increase in the number of light impulses in response to the stimulator is indicative of a reduced
ability of granulocytes to respond to nFMLP,
whereas an over 13-fold rise points to a high
response.
The frequency of low, normal and high indexes
observed in the control and studied groups, is
shown in Table 4 and in Fig. 1. The x2-test showed
that there is a significantly different frequency of
the number of normal results in the groups of sick
children (x2 /27.8757, P /3.382E/3 for 6 degrees of freedom). The smallest changes in the
ability of granulocytes to emit light as the result of

Table 1 Number of leucocytes and granulocytes in peripheral blood of studied children

Group

Leukocytosis in 1 ml blood

Granulocytes (%)

Number of granulocytes in 1 ml blood

Controls (n/15)
T (n /7)
I (n /12)
TI (n/16)

62269/1222
76289/2951
72009/2697
64169/1317

61.99/5.30
55.69/13.75
46.19/10.60
55.09/7.04

38999/881
45089/3108
33459/1768
34399/818

The results are expressed as mean value9/standard deviation (SD). Group T: children with idiopathic tonsillar
hypertrophy (without recurrent upper respiratory tract infection), group I: children without tonsillar hypertrophy
but with recurrent upper respiratory tract infection, group TI: children with tonsillar hypertrophy and with
recurrent upper respiratory tract infection.

368

M. Kowalska et al.

Table 2 The individual results obtained in studied groups of patients, presented as the mean value of the number
of light impulses emitted by a single cell before (sp, spontaneous chemiluminescence) and after stimulation (st,
stimulated chemiluminescence)
Chemiluminescence (impulse9/SD/min/cell)
Controls

TI

sp

st

ix

sp

St

ix

sp

st

ix

sp

st

ix

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16

2.190
1.550
1.060
1.160
0.68
1.400
0.860
1.190
1.250
2.460
0.760
1.290
1.170
2.020
1.410

9.070
7.030
4.960
5.760
3.47
5.900
4.730
6.560
7.330
14.490
5.440
9.320
12.750
24.100
19.65

3.14
3.53
3.67
3.96
4.10
4.17
4.50
4.51
4.86
4.89
6.15
6.22
9.89
10.93
12.94

13.560
3.660
0.470
1.970
0.690
10.970
0.630

12.240
19.260
2.640
16.130
48.970
361.0
4.690

0
4.28
4.61
7.18
69.97
31.9
6.44

0.970
8.760
8.450
7.740
44.190
2.330
1.060
0.950
2.850
2.470
5.890
1.850

0.650
10.900
10.660
10.420
83.540
10.010
6.150
6.01
38.300
52.000
138.40
85.600

0
0.24
0.26
0.34
0.89
3.33
4.8
5.33
13.4
20.0
22.6
45.5

3.25
0.380
0.620
7.510
5.970
4.310
13.440
1.200
1.640
1.290
23.200
1.630
0.970
1.040
0.600
0.740

4.01
3.820
6.710
8.100
10.530
9.010
37.600
2.860
13.410
22.200
55.600
56.100
34.00
38.4
36.300
79.400

0.23
0.38
0.62
0.7
0.76
1.09
1.8
2.33
7.15
16.2
23.2
32.0
33.9
35.9
59.5
106

Mean
SD

1.35
0.51

9.37
5.95

5.73
2.77

4.56
5.42

66.41
130.79

17.67
25.36

7.30
12.02

37.72
43.76

9.54
13.97

3.29
3.36

26.07
22.84

20.16
29.05

The index of chemiluminescence is calculated by dividing st by sp chemiluminescence value /1.

respiratory bursts were found in children with

idiopathic tonsillar hypertrophy (T), who did not
have a tendency towards recurrent respiratory
tract infections. In children without throat lymphatic tissue hypertrophy but with recurrent infections (I), the number of low, normal and high
results had a similar distribution. In the group of
children with tonsillar hypertrophy and recurrent
infections (TI), the number of normal results was
least frequent (in only two of 16 children) but that
of low and high results was the same (seven of 16
children).

The results of bacteriological studies are given in

Table 5. Six and three potentially pathogenic
aerobic bacteria strains were isolated from the
surface and the core of tonsils in (TI) and (T)
groups, respectively. Normal oral saprophytes were
widely present in swabs in majority of investigated
subject. In both groups Staphylococcus aureus was
the most frequently encountered bacteria, followed by Haemophilus influensae and Streptococcus pyogenes. Moraxella catharalis was found as a
coexisting microflora in two (TI) patients. Pseudomonas aureginosa occurred in tonsil culture in one

Table 3 Comparison of the peripheral blood granulocyte ability to generate light impulses
Groups

Controls
T
I
TI

Chemiluminescence (impulse9/SD/cell)

Index st/sp9/SD

Spontaneous (sp)

Stimulated (st)

1.359/0.51
4.569/5.43
7.309/12.02
3.299/3.36

0.72
0.01
0.06

9.379/5.95
66.419/130.79
37.729/43.76
26.079/22.84

0.146
0.04
0.048

5.749/2.77
17.679/25.36
9.549/13.97
20.169/29.05

Results are presented as the mean value of the number of light impulses emitted by a single cell before (sp) and
after (st) stimulation. The index of chemiluminescence is calculated by dividing st by sp chemiluminescence value.
The study was performed in the following groups: control, healthy children; group T, patients with tonsillar
hypertrophy but without recurrent infections; group I, patients with recurrent infections without tonsillar
hypertrophy; group TI, patients with tonsillar hypertrophy and recurrent infections.

Dysfunction of peripheral blood granulocyte oxidative metabolism in children

369

Table 4 The number of low, normal, and high chemiluminescence indexes in the studied groups
Groups

Index of chemiluminescence

Controls
T
I
TI
Total

Below 2

Between 2 and 13

Over 13

Total number

0
1
5
7
13

15
4
3
2
24

0
2
4
7
13

15
7
12
16
50

Characteristics of patient populations: controls, healthy children; T, patients with idiopathic tonsillar
hypertrophy; I group, patients with recurrent upper tract infections without tonsillar hypertrophy; and TI group,
patients with recurrent upper tract infections and tonsillar hypertrophy.

(TI) patients. In few cases pathogens were isolated

only from tonsils core.

4. Discussion
Granulocytes play an exceptionally important
role in inducing the non-specific immune response.
By acting in synergy with antibodies and complement, granulocytes participate in protecting the
body from harmful microorganisms. The role of the
particular types of granulocytes (neutrophils, eosinophils, basophils) in the elimination of pathogens

has been well-elucidated [13]. The role of the cells

in this system is especially visible in persons with a
reduced number of, or impaired function of granulocytes, who are particularly prone to infections.
Our studies have dealt with the ability of
granulocytes to initiate the synthesis of reactive
oxygen species (ROS), which is evaluated by the
chemiluminescence test. ROS are known to play an
important role in the destruction of pathogens as
well as in regulating the immune response [12].
Reduced values of ROS may be a cause of improper
immune responses that may manifest clinically as
recurring infections.

Fig. 1 Frequency of low, normal and high indexes observed in studied group of children.

370

M. Kowalska et al.

Table 5 Observed frequency of the potentially pathogenic strains of bacteria, cultured from the surface and the
core of the tonsils in patients with idiopathic tonsillar hypertrophy (T) and children with recurrent upper tract
infections and tonsillar hypertrophy (TI)
Bacteria

Staphylococcus aureus
Haemophilus influensae
Moraxella catharalis
Streptococcus pyogenes
Staphylococcus pneumoniae
Pseudomonas aureginosa

Both reduced and elevated reactivity of granulocytes is an unfavourable situation. A depressed

response to a stimulus points to a reduced ability to
produce ROS, i.e. to an impaired ability to eliminate pathogens. Excessive activity of neutrophils
may, on the other hand, be related to effective
elimination of pathogens but at the same time,
excessive stimulation of granulocytes may lead to
damage to DNA in other cells and the bodys own
tissues [14,15]. Many centres have conducted
studies on the effect of various factors on the
ability of granulocytes to produce ROS. Our studies
on children with chronic tonsillitis have shown that
they had impaired granulocyte function manifested
in an increased or decreased production of ROS.
Suzuki et al. [16] studied the effect of long-term
physical stress on granulocyte function and found
that their oxidative potential increased in a group
of healthy young men subjected to intense training. An in vitro study [17] demonstrated that
tonsillar cells produce factors which activate
various neutrophil functions, including superoxide
production, and the activation correlates with the
course of inflammation in the tonsils. No information was available in the literature, about the
evaluation of chemiluminescence of peripheral
granulocytes in children with recurrent upper
respiratory tract infections and tonsillar hypertrophy.
Our studies conducted on three groups of patients (investigated at the time they had no clinical
and laboratory signs of infection) showed disorders
of granulocyte function in most of them, in terms
of neutrophil ability to synthesise free oxygen
radicals and the emission of light that accompanies
this reaction. Comparison of the results of the
three groups of studied children with those of
controls showed significant differences both in
spontaneous and stimulated chemiluminescence
and the calculated indexes. These changes manifested as increased or depressed granulocyte

TI (n/12)

T (n/5)

surface

core

surface

core

2
1
2
1
1
0

4
3
2
2
2
1

2
1

2
1

reactivity occurring with different frequencies in

the studied groups. The most distinct disorders
were observed in the group of children with tonsil
hypertrophy and recurrent infections (TI); an
abnormal response to stimulation with nFMLP was
found in about 90% of these children */low reactions was found in about 50%, and high reactions in
about 40%. The fewest abnormal responses were
observed in children with idiopathic tonsil hypertrophy (T); in about 30%, including 15% low and
about 15% high reactions. In the group of children
without tonsil hypertrophy, but with recurrent
infections (I), 75% of reactions were abnormal,
including 50% high and 25% low. Finding an abnormal response of granulocytes to stimulation in
children with idiopathic tonsil hypertrophy (T)
may suggest the involvement of the lymphoid
tissue of the tonsil in inducing granulocyte function
disorders. The results obtained in children without
tonsil hypertrophy but with recurrent upper respiratory tract infections (I) may suggest a causative role of infections in disorders of producing ROS
in granulocytes */immunological alteration secondary to infections, or alternatively, explain the
occurrence of recurrent infections by the abnormal
function of these cells. The coexistence of two
unfavorable factors (tonsil hypertrophy and infection) leads to a higher frequency of disorders of
chemiluminescence, which is supported by observations on the group of children in whom concomitant tonsil hypertrophy and recurrent upper
respiratory tract infections (TI) were found.
We found no correlation between the presence
of a certain bacterial strain in the tonsil tissue and
altered granulocyte ability to produce ROS,
although a relatively small number of investigated
patients may influence this result. Bacteria, which
colonised the tonsils may be, on the one hand a
source of the continuous antigenic stimulation,
what may be the reason for hyper-reactivity of
granulocytes (abnormally high response to nFMLP).

Dysfunction of peripheral blood granulocyte oxidative metabolism in children

On the other hand, it is well established that many

bacterial products may disturb various granulocytes functions; Enterobacter cloacae leukotoxin,
cholera and pertussis toxins may decrease the
neutrophil ability to produce ROS [18,19].
Although, the lack of ROS production by nFMLPstimulated granulocytes in our patients should be
rather treated as the reason for recurrent infections, the potential inhibition of the granulocytes
function by the bacterial products cannot be ruled
out.
Further studies will be undertaken to explain the
causes of the granulocyte disorders. They will
include an evaluation of the membrane and cytoplasmic proteins responsible for the proper function of these cells.

[8]

[9]

[10]

[11]

[12]

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