24 KUBÁŇ, ĎURČ, LAČNÁ, GREGUŠ, FORET, ET AL.

The use of MII-pH is, however, rather unpleasant and up

to one third of subjects report discomfort. In this paper,

the replacement of the above-mentioned MII-pH method

with a significantly less invasive technique for analyzing

EBC was attempted. EBC was collected using a specially

designed miniature sampler [4, 9, 10] that was previously

developed in our laboratory. EBC samples were collected

from several healthy volunteers and a group of patients

suffering from symptoms attributed to gastroesophageal

reflux disease. Capillary electrophoresis was used to ana-

lyze the ionic content of EBC samples and differences in

selected ion concentrations were identified between the

groups.

2. Experimental

2.1 Instrumentation

An in-house-built CE instrument was used for all elec-

trophoretic separations at ± 15 kV using a high voltage

power supply unit (Spellman CZE2000R Start Spellman,

Pulborough, UK). Two Pt wires (with an outer diameter

(OD) of 0.5 mm, 3 cm in length, Advent Research Ma-

terials Ltd., Eynsham, UK) were inserted into the elec-

trolyte vials to serve as electrodes. Fused-silica (FS) cap-

illaries (with an inner diameter (ID) of 50 µm, OD of

375 µm, 39 cm in total length, Polymicro Technologies,

Phoenix, AZ, USA) were used for the separation. All CE

experiments were performed at ambient temperature. A

custom-made contactless conductometric detector (CCD)

(Version 5.06, ADMET s.r.o., Prague, Czech Republic)

operating at a frequency of 1.8432 MHz and a voltage of

50 Vp−p was used for the detection of the separated ana-

lytes. Data were collected using an Orca 2800 24-bit A/D

converter and ECOMAC software ver. 0.254 (ECOM spol

s.r.o., Prague, Czech Republic). In all experiments, hy-

drodynamic injection was applied to the samples, con-

sisting of the elevation of the sample vial to a height of

10 cm for 20 s.

The sampler for the collection of EBC has been de-

veloped in our group previously [9]. Briefly, it was con-

structed from a 2 ml syringe (B. Braun Melsungen AG,

Melsungen, Germany) cooled by a 5 cm-long hollow alu-

minum cylinder with an OD of 2.5 cm and an ID identical

to the OD of the syringe (see Fig. 1).

The cylinder was kept in dry ice at -80 °C prior to

the collection of EBC and an insulation sleeve was used

during its collection. A straw with an OD of 6 mm, and a

wall thickness of 0.2 mm (purchased in a local store) was

used to exhale the air through the sampler. The end of the

syringe was enclosed with a parafilm septum to avoid loss

of EBC.

2.2 Chemicals

All chemicals were of reagent grade (Sigma-Aldrich,

Steinheim, Germany) and deionized (DI) water (Purite,

Figure 1: The photograph and scheme of the EBC sampler

used in this work.

Neptune, Watrex, Prague, Czech Republic) was used for

the preparation of stock solutions and dilutions. Back-

ground electrolytes (BGEs) for CE measurements were

prepared daily by diluting 100 mM of stock solutions of

2-(N-morpholino)ethanesulfonic acid (MES), L-histidine

(L-His) and 18-Crown-6 to the required concentrations.

Cetyltrimethylammonium bromide (CTAB) was prepared

as a 10 mM stock solution in 5 % acetonitrile.

The separation electrolyte that was used for separa-

tion and quantitation of inorganic anions, cations and or-

ganic acids consisted of 20 mM MES, 20 mM L-His, 2

mM 18-Crown-6 and 30 µM CTAB.

2.3 Capillary-conditioning procedure

Prior to its first use, the separation capillary was precon-

ditioned by flushing it with 0.1 M NaOH for 30 mins.,

then with DI water for 30 mins. and finally with a solu-

tion of BGEs for 10 mins. Between two successive injec-

tions, the capillary was flushed with the BGE solution for

1 min. At the end of a working day, the capillaries were

washed with DI water for 15 mins., followed by the ap-

plication of a vacuum for 5 mins. before being stored dry

overnight.

2.4 Sample-collection procedure

The EBC was collected in the morning, the subjects did

not eat or drink beforehand. The EBC was collected using

the previously described EBC-sampler. The subject was

asked to exhale deeply 3-5 times into the sampler, but

depending on the lung capacity of each, the number of

exhalations was modified to collect approximately 100 µl

of their EBC. After the sampling of EBC was completed,

the condensate from the walls of the syringe was forced

to the tip of the syringe by the plunger and transferred to

the sample vial for CE analysis. Part of the EBC sample

was also used in another experiment published elsewhere,

in which the pH was measured using a microelectrode.

Hungarian Journal of Industry and Chemistry



CE ANALYSIS OF EBC IN GERD DIAGNOSIS 25

Figure 2: Separation of a model mixture consisting of 4 in-

organic anions and 4 organic acids. BGE: 20 mM MES/L-

His, 2 mM 18-Crown-6, 30 µM CTAB. HV: positive +15

kV, C4D detection. Ion concentrations in the parentheses

in µM: acetate (200); chloride, nitrate, lactate, propionate,

butyrate (25); nitrite, sulfate (10).

2.5 Selection of patients and healthy individ-
uals

In this initial screening, a group of healthy individuals

and a group of patients diagnosed with asthma and pul-

monary fibrosis were selected. The healthy individuals

had no history of GERD or heartburn and were free from

other related symptoms. The healthy individuals selected

were from approximately the same age group as the pa-

tients, i.e., the average age of healthy subjects was 48 and

that of patients was 56. The patients suffered from asthma

and pulmonary fibrosis and were from the Department of

Pulmonary Diseases and Tuberculosis at the Faculty Hos-

pital Brno.

3. Results and Analysis

3.1 Electrolyte selection

To separate the ionic content of the EBC, the BGEs

composed of MES and L-His was chosen as this elec-

trolyte allows for the analysis of anions, organic acids,

and cations with good degrees of sensitivity. MES and L-

His fulfill the criteria for suitable coions and counterions

in CE separation using contactless conductivity detection

(C4D). The conductance of the respective BGE compo-

nents is low, thus analytes including small organic acids

(acetate, lactate, butyrate) will be detected as positive

peaks. The addition of 18-Crown-6 to the separation elec-

trolyte improves the resolution of K+ and NH
+
4 cations

Figure 3: Separation of a model mixture of 5 inorganic

cations. BGE: 20 mM MES/L-His, 2 mM 18-Crown-6, 30

µM CTAB. HV: negative -15 kV, C4D detection. Ion con-

centrations in the parentheses in µM: ammonium (1000);

calcium (25); potassium, sodium and magnesium (10).

and does not influence the selectivity of other measured

cations to a great extent, nor does it influence the sepa-

ration of anions and organic acids. CTAB is added to the

separation electrolyte to decrease the electroosmotic flow

(EOF).

It should be noted here that although this separation

electrolyte allows for the simultaneous separation of an-

ions and cations using dual-opposite end injection [11], in

this work anions and cations were determined separately

by switching the high-voltage polarity. The separation of

a model mixture consisting of 8 anions in less than 2.5

mins. is shown in Fig. 2.

The ion concentrations were selected to be similar to

those found in EBC samples. The separation of cations

using the same conditions but using reverse-polarity volt-

age is shown in Fig. 3. The ammonium cation is usually

present at a concentration 100 times greater than other

cations in the EBC, its concentration was thus also in-

creased to 1000 µM to reflect the expected concentration.

Note that even with this significant excess the separation

of NH
+
4 from K

+ is sufficient and the BGE composition

can be used for real sample analysis.

3.2 Analysis of anions in EBC samples

From each subject, the EBC sample was collected as de-

scribed previously. About 50 µl of the sample was trans-

ferred into an Eppendorf tube and hydrodynamically in-

jected into the CE system. The EBC samples were ana-

lyzed first for anions and organic acids using positive HV

polarity and then for cations using negative HV polarity,

46(1) pp. 23-27 (2018)



26 KUBÁŇ, ĎURČ, LAČNÁ, GREGUŠ, FORET, ET AL.

Figure 4: Separation of anions in EBC samples of healthy

persons as well as patients with acid reflux or weakly acid

reflux. BGE: 20 mM MES/L-His, 2 mM 18-Crown-6, 30

µM CTAB. HV: positive +15 kV, C4D detection.

with the HV electrode placed in the detection vial. The

concentrations of all 13 ions in the samples were eval-

uated using calibration curves measured with standard

solutions. The parameters such as the calibration curve,

regression coefficient (R2) and concentration range are

shown in Table 1. In this initial screening the analysis of

several samples from the healthy group and patients that

were diagnosed as having the acid reflux or weakly acid

reflux was attempted and the ions that would be signifi-

cantly different in these groups identified.

A series of electropherograms of anions and organic

acids in a healthy individual, patient with acid reflux and

patient with weakly acid reflux is shown in Fig. 4. One

can clearly see that the concentrations of several anions,

most notably chloride, nitrate and organic acids, are sig-

nificantly higher in the group of patients than in that of the

healthy volunteers. Some small inorganic anions such as

nitrite and nitrate are often found in the EBC of patients

with respiratory diseases as markers of nitrosative stress.

On the other hand, the presence of an increased concen-

tration of chloride and organic acids may be a significant

step towards the diagnosis of GERD.

3.3 Analysis of cations in EBC samples

The analysis of cations in the same samples can be seen

in Fig. 5. Although higher concentrations of the ammo-

nium cation were found in patients compared to healthy

individuals, the content was not significantly different

from that of healthy individuals, and this applied for other

cations (K+, Na+, Ca2+, Mg2+) as well.

Figure 5: Separation of cations in EBC samples of healthy

persons as well as those with acid reflux and weakly acid

reflux. BGE: 20 mM MES/L-His, 2 mM 18-Crown-6, 30

µM CTAB. HV: negative -15 kV, C4D detection.

4. Discussion

A limited number of subjects were tested and the determi-

nation of whether a simple EBC sample could be used as

a surrogate for more invasive, expensive and tedious diag-

nostic methods attempted. The analysis of anions showed

some promising results with regard to the small inorganic

anions (chloride and nitrate) collected and the concentra-

tion of organic acids that were elevated in the patients

Table 1: Calibration equations of all separated anions,

cations and organic acids. BGE: 20 mM MES/L-His, 2

mM 18-Crown-6, 30 µM CTAB. HV: positive +15 kV or

negative -15 kV, C4D detection.

Ion Calibration equation R
2 range

(µM)

Cl
−

y = 0.0278x + 0.0258 0.9957 0.6-25

NO
−

2
y = 0.0270x + 0.0023 0.9994 0.6-25

NO
−

3
y = 0.0315x + 0.0166 0.9987 0.6-25

SO
2−

4
y = 0.0656x + 0.0143 0.9980 0.25-10

acetate y = 0.0156x + 0.0200 0.9995 1-200

lactate y = 0.0207x + 0.0097 0.9996 0.6-25

propionate y = 0.0189x + 0.0024 0.9983 0.6-25

butyrate y = 0.0188x − 0.0001 0.9990 0.6-25

NH
+

4
y = 0.0211x − 0.1437 0.9993 25-1000

K
+

y = 0.0347x + 0.0013 0.9994 0.25-10

Ca
2+

y = 0.0528x + 0.0059 0.9995 0.6-25

Na
+

y = 0.0356x + 0.0079 0.9996 0.25-10

Mg
2+

y = 0.0618x − 0.0054 0.9995 0.25-10

Hungarian Journal of Industry and Chemistry



CE ANALYSIS OF EBC IN GERD DIAGNOSIS 27

suffering from GERD symptoms, compared to healthy

volunteers. Unfortunately, with regard to the analysis of

cations, the differences were not significant and cations

were deemed unsuitable.

5. Conclusion

Capillary electrophoretic analysis of EBC was used for

the first time in an attempt to distinguish the groups of

patients with GERD from healthy individuals. CE with

C4D was used for the analysis of small inorganic anions,

cations and organic acids present in the EBC samples.

Although it has been shown that selected samples had

elevated concentrations of chloride, nitrate, butyrate and

propionate, the number of subjects was too small to draw

definite conclusions concerning the discriminatory power

of these ions. It also seems that although there is a dif-

ference between groups of healthy individuals and suf-

ferers of acid reflux/weakly acid reflux, the results with

regard to acid reflux and weakly acid reflux are very sim-

ilar and these two groups cannot be distinguished based

on the current data. A larger scale clinical study, in which

the EBC of patients and healthy individuals is scrutinized

with regard to the ion content, pH and concentration of

other biomarkers (for instance pepsin in saliva) to obtain

statistically significant results for evaluation is currently

being undertaken. Nevertheless, the initial data is some-

what promising for EBC as a useful non-invasive alterna-

tive for other methods used in GERD diagnostics.

Symbols

BGE background electrolyte

CE capillary electrophoresis

C4D contactless conductivity detection

CTAB cetyltrimethylammonium bromide

DI deionized

EBC exhaled breath condensate

GERD gastroesophageal reflux disease

L-His L-histidine

ID inner diameter

MES 2-(N-morpholino)ethanesulfonic acid

OD outer diameter

Acknowledgement

This research was supported by grant no. 17-31945A

from the Ministry of Health of the Czech Republic.

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46(1) pp. 23-27 (2018)


	 Introduction
	 Experimental
	 Instrumentation
	 Chemicals
	 Capillary-conditioning procedure
	 Sample-collection procedure
	 Selection of patients and healthy individuals 

	 Results and Analysis
	 Electrolyte selection
	 Analysis of anions in EBC samples
	 Analysis of cations in EBC samples

	 Discussion
	 Conclusion