capnography in spontaneously breathing preterm infants with bronchopulmonary dysplasia

Pediatric Pulmonology 46:896–902 (2011)

Capnography in Spontaneously Breathing PretermInfants With Bronchopulmonary Dysplasia

Emmanuel Lopez, MD, PhD,1,2* Jihene Mathlouthi, MD,1 Sandra Lescure, MD,1,2

Baruch Krauss, MD, EdM,3,4 Pierre-Henri Jarreau, MD, PhD,1,2,5 and Guy Moriette, MD1,2,5

Summary. Background: In adult patients with chronic obstructive pulmonary disease, there is

a gradient between end-tidal carbon dioxide (EtCO2) and arterial carbon dioxide pressure

(PaCO2), and the slope of the ascending phase of the capnogram is decreased due to obstruc-

tion. Corresponding data are lacking in infants with bronchopulmonary dysplasia (BPD). Objec-

tives: To compare PCO2–EtCO2 gradient and capnogram shape in two groups of

spontaneously breathing preterm subjects: infants with BPD and infants without respiratory

disease (controls). Material and Methods: Capnography was performed at 36 weeks post-

menstrual age in 20 infants (12 BPD with oxygen dependency, 8 controls). Respiratory rate

and the components of the respiratory cycle were measured. The PCO2–EtCO2 gradient was

calculated using EtCO2 values and simultaneously sampled capillary values (PcCO2). Capno-

grams were compared between groups. Results: In BPD subjects, respiratory rate was

increased (60 � 16 bpm vs 43 � 16 bpm, P ¼ 0.009); a widened PcCO2–EtCO2 gradient was

observed (13 � 4 mmHg vs 0 � 7 mmHg, P ¼ 0.0013); the ascending phase of the capno-

gram was not decreased, whereas the initial inspiratory phase was prolonged (0.32 � 0.05 vs

0.24 � 0.04, P ¼ 0.001). Conclusions: Compared with healthy infants, a higher PcCO2–EtCO2

gradient was observed in infants with BPD, suggesting that ventilation–perfusion mismatch

may be present in these infants. The capnogram did not exhibit the characteristic shape of

airway obstruction. Pediatr Pulmonol. 2011; 46:896–902. � 2011 Wiley-Liss, Inc.

Key words: preterm infant; bronchopulmonary dysplasia; capnogram; dead space.

Funding source: none reported.

INTRODUCTION

Bronchopulmonary dysplasia (BPD) occurs inapproximately 20% of premature infants who requiremechanical ventilation and oxygen therapy for acuterespiratory distress.1 This chronic lung disease resultsfrom injury characterized by abnormal lung structureincluding inflammatory changes, interstitial fibrosis,edema, atelectasis, and narrowed small airways.2

Alveoli are fewer and larger, and the overall surfaceavailable for gas exchange is reduced. Growth, struc-ture, and function of pulmonary circulation are alsoreduced.3

These changes result in ventilation–perfusion mis-match, increased dead space ventilation, decreasedcompliance, and increased airway resistance.1 Sub-sequently, in infants with BPD, compared with healthypreterm infants, forced expiratory flows remaindecreased over the first 3 years,4 or even the first 7 yearsof life.5 More recently, airflow limitations have beenconfirmed in preterm infants with BPD in a prospectivelongitudinal study performed in the era of surfactant.6

BPD is a form of obstructive lung disease. In adultswith chronic obstructive pulmonary disease, the

1AP-HP, Groupe Hospitalier Cochin-Saint Vincent de Paul, Service de

Medecine Neonatale de Port-Royal, Paris, France.

2PremUP, Paris, France.

3Division of Emergency Medicine, Children’s Hospital, Boston.

4Department of Pediatrics, Harvard Medical School, Boston,

Massachusetts.

5Faculte de Medecine, Universite Paris Descartes, Paris, France.

Deltamedics, France, provided technical support. Baruch Krauss MD,

EdM is a consultant for Oridion Medical, a capnography company, and

holds two patents in the field of capnography.

*Correspondence to: Emmanuel Lopez, MD, PhD, Groupe Hospitalier

Cochin-Saint Vincent de Paul, Service de medecine neonatale de Port-

Royal, 123 Boulevard de Port-Royal, 75014 Paris, France

E-mail: [email protected]

Received 15 June 2010; Revised 12 February 2011; Accepted 15 Febru-

ary 2011.

DOI 10.1002/ppul.21445

Published online 4 April 2011 in Wiley Online Library

(wileyonlinelibrary.com).

� 2011 Wiley-Liss, Inc.

capnogram has a characteristic shape that differs fromthat of subjects with normal lung function: the take-offangle of the ascending phase is decreased and thealveolar plateau elevation angle is increased in patientswith obstructive lung disease compared with normalsubjects.7 These differences in shape increase with dis-ease severity.7 The influence of BPD-associated airwayobstruction on the capnogram has not been studied inpreterm infants.

We have previously assessed the accuracy of side-stream capnography in ventilated preterm infants8 andreported the presence of a gradient between carbondioxide pressure (PCO2) and end-tidal carbon dioxide(EtCO2) in preterm infants ventilated for lung disease.The present study was performed in two groups ofspontaneously breathing infants: preterm infants withBPD and healthy preterm infants. We hypothesized that,in preterm infants with BPD, compared with healthypreterm infants: (i) a wider PcCO2–EtCO2 gradientand (ii) characteristic alterations of the capnogramexpiratory phase, reflecting airway obstruction wouldbe observed.

METHODS

Patient Population

The study was conducted in a prospective, non-randomized manner using a sample of spontaneouslybreathing preterm infants admitted to the Service deMedecine Neonatale, Groupe Hospitalier Cochin-SaintVincent de Paul in Paris, France, over a 9-month period(from July 2007 to March 2008). Infants were eligiblefor inclusion in the study when the gestational age atbirth was 37 weeks or less, and when the infant’s post-menstrual age (PMA) at the time of the study wasbetween 36 and 40 weeks. Preterm infants requiringsupplemental oxygen in order to maintain oxygen satur-ation between 90% and 95% at 36 weeks of PMA9

were included in the BPD group. Supplemental oxygenwas provided by nasal cannulas, using gas flows (mix-ing air and oxygen) of 1–1.5 L/min. Preterm infantswithout supplemental oxygen were included in the con-trol group. Infants were included consecutively. Infantswith congenital diaphragmatic hernia, congenital heartdisease, neuromuscular disease, thoracic wall deform-ities, or sepsis were excluded. The institutional researchethics committee approved the study. Parents were

provided with information about the study and consentwas obtained for each patient.

End-Tidal Carbon Dioxide Monitoring

Capnography was performed using a portable side-stream device, Capnostream-20TM (Oridion Medical,Needham, Massachusetts) utilizing low-flow Micro-streamTM sampling technology.8,10,11 The capnographcollects a continuous sample of gas at a flow rate of50 ml/min and records the instantaneous CO2 concen-tration every 40 ms at a printer speed of 25 mm/sec.During recording, patients were sleeping in the proneposition with a CO2 sampling cannula inserted in thenose. In BPD patients, two nasal cannulas were used(EtCO2 and oxygen cannulas). Fixation of the EtCO2

nasal cannula was similar to that of the routinely usednasal oxygen cannula. Recordings were performed onlywhen CO2 waveforms were deemed visually similar tothose previously reported11 thus confirming appropriateposition of EtCO2 nasal cannula.The possible effect of additional air flow on the

measured EtCO2 level was assessed by measuringEtCO2 in the presence and in the absence of 1.5 L/minair flow provided by nasal cannulas in five infants notparticipating in the study, born at 36 weeks of gesta-tional age or above, and free of any pulmonary disease(no BPD). Their gestational age and birth weightwere 36.9 � 1.2 weeks and 2455 � 296 g, respectively(mean � SD). EtCO2 levels were similar with or with-out additional air flow (35.4 � 4 mmHg vs 36.4 �5.3 mmHg, P ¼ 0.91).Infants were studied in the prone position in both the

BPD and control groups. Although patients are usuallystudied in the supine position, the prone position waschosen because the usual guidelines in our unit indicatethat infants with BPD should be preferably nursed inthe prone position to improve pulmonary mechanics,oxygenation, and to reduce thoracoabdominal asyn-chrony. Infants are subsequently placed in the supineposition prior to discharge. The study was performedwhen infants were not receiving feeds or medication.

Waveform Analysis

The waveforms were printed out, scanned and down-loaded to Adobe Photoshop1 software. The major fea-tures of the capnogram were analyzed. The inflectionpoints in CO2 concentration were detected, correspond-ing to the start of inhalation and the end of exhalation,for each breath. Within a breath, the linear phases ofthe capnogram were identified, including the initialexpiratory rise and the alveolar plateau. Angles fromthe horizontal were calculated using Adobe Photoshop1

software, including the take-off angle of the initialexpiratory rise and the elevation angle for the slope of

ABBREVIATIONS:

BPD bronchopulmonary dysplasia

PcCO2 carbon dioxide capillary pressure

EtCO2 end-tidal carbon dioxide

Capnography in Bronchopulmonary Dysplasia 897

Pediatric Pulmonology

the alveolar plateau. A sample, containing at least eightspontaneous breaths over a period of 15 sec, was col-lected from each patient and the mean and standarddeviation were calculated.7

In each patient, quantitative waveform parameterswere analyzed, as previously described in adults7

(Fig. 1): initial expiratory phase (AB), take-off angle(a), expiratory plateau (BC), elevation angle for theslope of the alveolar plateau (b), initial inspiratoryphase (CD), inhalation trough (DE), expiratory time(Te ¼ AC), inspiratory time (Ti ¼ CE), respiratorycycle total time (Ttot or AE).

Since patients with BPD have higher than normalrespiratory rates, these measurements were related torespiratory cycle duration (Ttot), in order to assess theinfluence of BPD on waveform parameters independ-ently of respiratory rate. The following ratios weremeasured: AB/Ttot, BC/Ttot, CD/Ttot, DE/Ttot, Ti/Ttot, and Te/Ttot. Capnogram shape was comparedin preterm infants with BPD and in preterm infantswithout pulmonary disease.

Blood Sampling and Clinical Data Collection

A capillary blood gas sample was taken from eachpatient (just after EtCO2 recording, in the prone pos-ition) to measure the capillary pressure of CO2 (PcCO2)and evaluate the PcCO2–EtCO2 gradient. Oral sucrosewas given to relieve procedural pain and to avoid cryingor apnea during blood sampling which could affect thePcCO2 level. PcCO2 was used as a proxy for the goldstandard arterial pressure of CO2 (PaCO2). A good cor-relation has been demonstrated between PcCO2 andPaCO2 in infants.12 Blood pressure, body weight, heartrate, blood gas parameters, and respiratory rate werealso recorded and compared between groups.

Statistical Analysis

The sample size was calculated on the basis ofprevious data on the EtCO2–PaCO2 gradient:11 eightinfants per group was considered sufficient to detect adifference of 4 mmHg between healthy infants andinfants with lung disease with 80% power for a type 1error of 5%. All parameters were expressed as means(SD) or medians (interquartile), and were comparedusing Mann–Whitney test or analysis of variance(Statview1, California, USA). A P-value < 0.05 wasconsidered significant.

RESULTS

Twenty-one patients were eligible for this study.Capnogram analysis was not possible in one of theseinfants due to technical problems. Data were thereforecollected and analyzed for 20 patients: 12 preterminfants with BPD and 8 late preterm infants withoutBPD. Eight capnograms were collected from eachpatients and a total of 160 capnograms were analyzedas previously described. All parents consented toparticipation of their infant. No infant was excludedbecause of a change in EtCO2 induced by air flow. Noinfant presented apnea of prematurity, cerebral lesions,and pulmonary hypertension. Eight of twelve infants inthe BPD group had moderate BPD (FiO2 0.22–0.29delivered by oxygen nasal cannula at 36 weeks ofPMA). The remaining four infants had severe BPD(FiO2 > 0.30 at 36 weeks of PMA). PMA and weightwere not significantly different between the BPD groupand the control group, while postnatal age and gesta-tional age at birth were significantly different due to thestudy design (Table 1). In the BPD group, respiratoryrate and heart rate were higher and pH was lower. Basedeficit and mean arterial pressure were similar in thetwo groups.

PcCO2–EtCO2 Gradient

Mean PcCO2–EtCO2 gradient was significantly higherin the BPD group compared with the control group,(13 � 4 mmHg vs 0 � 7 mmHg, P ¼ 0.001) (Table 1,Fig. 2) as although PcCO2 was significantly higher inthe BPD group (50 � 8 mmHg vs 38 � 5 mmHg,P ¼ 0.002), EtCO2 was similar in the two groups(37 � 8 mmHg vs 40 � 3 mmHg, P ¼ 0.35).

Waveform Analysis

The capnogram shape of the BPD group differedfrom that of adults with COPD and from that of thecontrol group (Fig. 3).Fifteen quantitative waveform parameters were

measured (Table 2). Due to increased respiratory rate inthe BPD group, expiratory (AC, Fig. 1) and inspiratory

Fig 1. The normal time-based capnogram in adults showing

phases A–E and take-off and elevation angles. AB: initial expir-

atory phase, BC: expiratory plateau, AC: expiratory time (Te),

CD: initial inhalation phase, DE: inhalation trough, CE: inspira-

tory time (Ti), a: take-off angle, b: elevation angle for the slope

of the alveolar plateau, AE: respiratory cycle total time (Ttot).

898 Lopez et al.


phases (CE, Fig. 1) were both significantly diminished.In order to take into account the effects of respiratoryrate, each waveform parameter value was related toduration of the respiratory cycle (Ttot).

No difference in expiratory phase parameters wasobserved between BPD infants and control infants, (A–C, Fig. 1), as the durations of the initial expiratoryphase (AB/Ttot) and alveolar phase (BC/Ttot) weresimilar in the two groups (Table 2).

In contrast, significant differences were observed forinhalation phase parameters (CE, Fig. 1), as the initialinhalation phase (CD/Ttot) was longer in BPD patients,while the second part of the inhalation phase (DE/Ttot)was shorter (Table 2).

DISCUSSION

Low-flow sidestream capnography8,11 was used inspontaneously breathing infants, to compare PcCO2–EtCO2 gradient and capnogram shape in infants withBPD and control subjects. Infants with BPD, comparedwith controls, exhibited an increased gradient, no differ-ence in exhalation phase parameters, and significantmodifications of inhalation phase characteristics. This isthe first study to characterize capnogram shape in spon-taneously breathing preterm infants with BPD.The capnogram of spontaneously breathing preterm

infants has been previously described,13 including theabsence of expiratory plateau, a finding which has beenexplained by high respiratory rate, low tidal volume,and ventilation–perfusion mismatch.14 In the presentstudy, an expiratory plateau was observed on capno-grams of spontaneously breathing preterm infants. Thiscould be due to the use of a new generation of capno-graph with low-flow MicrostreamTM technology. Theabsence of PcCO2–EtCO2 gradient in our healthycontrol subjects provides additional support for theaccuracy of this technology in this category of infants.In contrast, EtCO2 did not increase with PcCO2 ininfants with BPD, resulting in a PcCO2–EtCO2 gradientwhich could result from increased dead space15 andventilation–perfusion mismatch,1 as alteration of lungfunction related to BPD results in increased dead spaceventilation due to high respiratory rate and shallowbreathing. Inspired gas may be distributed to poorlyperfused areas of the lung, worsening ventilation–perfusion mismatch.16 Patients with BPD also presentan increased right-to-left shunt.17 The influence of

TABLE 1—Clinical Characteristics

Control (n ¼ 8) BPD (n ¼ 12) P-value

PMA at study (week) 36.9 � 0.8 36.7 � 1.1 0.21

Weight at study(g) 2277 � 240 2037 � 446 0.14

Postnatal age (d) 13 � 9 63 � 16 0.0002

Gestational age at birth (week) 35.4 � 1.6 27.6 � 1.4 0.0001

Prenatal steroids, n (%) 5 (62) 9 (75) 0.55

Postnatal surfactant, n (%) 0 (0) 12 (100) <0.0001

Mechanical ventilation (d) 0 � 0 21.6 � 11.4 0.0002

CPAP (d) 0.2 � 0.4 33.2 � 5.6 0.0002

Anemia of prematurity 4 (50) 12 (100) 0.006

Caffeine treatment, n (%) 0 (0) 4 (33) 0.06

Heart rate (bpm) 143 � 6 157 � 14 0.02

Mean arterial pressure (mmHg) 48 � 6 53 � 5 0.09

pH 7.39 � 0.03 7.34 � 0.03 0.01

Base deficit �1 � 1.5 0.1 � 2 0.22

Respiratory rate (c/min) 43 � 16 60 � 16 0.009

PcCO2 (mmHg) 38 � 5 50 � 8 0.002

EtCO2 (mmHg) 40 � 3 37 � 8 0.35

PcCO2–EtCO2 (mmHg) 0 � 7 13 � 4 0.0009

Values are expressed as mean (SD) and median (interquartiles) for PcCO2–EtCO2.

CPAP indicates continuous positive airway pressure.

Fig 2. The PcCO2–EtCO2 gradient calculated in the control

and BPD groups. Values are medians (interquartile). �P < 0.01,

compared with values obtained in the control group.



parenchymal lung disease and ventilation–perfusionmismatching on PCO2–EtCO2 gradient has been pre-viously studied in ventilated preterm infants.8 Newbornswith pulmonary disease presented a higher gradientbetween EtCO2 and PaCO2, compared to newbornswithout pulmonary disease,11 who present a ‘‘normal’’gradient, defined as 0–5 mmHg.18 Kugelman et al.19

found that the correlation between distal EtCO2 andPaCO2 decreased with the severity of lung disease,but the gradient remained <5 mmHg in patients withsevere lung disease. A similar gradient has also beenreported in spontaneously breathing adult patientswith COPD, in whom the PaCO2–EtCO2 gradientwas correlated with the degree of obstruction

(8.2 � 5.6 mmHg).20 In this study, we could not assessthe correlation between PaCO2 and EtCO2 gradient andseverity of BPD due to the small number of infants withsevere BPD. The possible value of the PaCO2–EtCO2

gradient to assess severity of BPD or exacerbationstherefore remains a matter of speculation.Capnogram differences were observed between BPD

patients and controls. However, these differences weremarkedly different from those observed in adults withCOPD, as a reduced slope of the capnogram ascendingphase and an increased elevation angle of the expiratoryplateau have been reported in COPD patients comparedwith normal subjects. These abnormalities are due toobstructive lung disease, as decreased flow rates result

Fig 3. A: A sample capnogram recorded in a preterm infant without BPD. B: A sample capno-

gram recorded in a preterm infant with BPD. C: A sample capnogram recorded in adult with

COPD (figure adapted from Krauss et al.7).

TABLE 2—Waveform Parameters

Waveform parameters (1 mm ¼ 0.04 sec) Control (n ¼ 8) BPD (n ¼ 12) P-Value

RR (bpm) 43 � 16 60 � 16 0.009

AE-Respiratory cycle total time (Ttot) (sec) 1.58 � 0.48 1.18 � 0.40 0.005

AC-Expiratory time (Te) (sec) 0.92 � 0.28 0.60 � 0.24 0.009

CE-Inspiratory time (Ti) (sec) 0.66 � 0.26 0.54 � 0.12 0.02

Expiratory phase

AB-initial expiratory phase (sec) 0.44 � 0.10 0.32 � 0.06 0.0003

BC-alveolar phase (sec) 0.38 � 0.30 0.28 � 0.14 0.14

a-Take-off angle (degrees) 42 � 4 48 � 6 0.02

b-Elevation angle (degrees) 1.1 � 1.4 0.7 � 0.9 0.41

Inhalation phase

CD-Initial inhalation phase (sec) 0.40 � 0.06 0.36 � 0.10 0.58

DE-Inhalation trough (sec) 0.30 � 0.22 0.17 � 0.12 0.007

Waveform parameters standardized for RR

Expiratory phase

Te/Ttot 0.53 � 0.11 0.53 � 0.06 0.64

AB/Ttot-initial expiratory phase/Ttot 0.27 � 0.08 0.27 � 0.06 0.24

BC/Ttot-alveolar phase/Ttot 0.23 � 0.11 0.25 � 0.09 0.75

Inhalation phase

Ti/Ttot 0.46 � 0.11 0.46 � 0.06 0.64

CD/Ttot-initial inhalation phase/Ttot 0.24 � 0.04 0.32 � 0.05 0.001

DE/Ttot-inhalation trough/Ttot 0.08 � 0.04 0.05 � 0.02 0.01

Values are expressed as median (interquartile).

900 Lopez et al.


in decreased slope of the ascending phase. The charac-teristic slope of the alveolar plateau is induced by exha-lation from unequally ventilated alveoli with differentCO2 concentrations.7 The capnogram abnormalitiesreported in COPD are of clinical significance, as theyare correlated with reduced forced expiratory volume in1 sec.7

The expiratory phase data obtained in infants withBPD did not differ from those obtained in controlinfants but differed from those obtained in adult COPDpatients, as the absence of a decreased slope of theinitial expiratory phase suggests that infants with BPDdo not exhibit increased airway resistance, althoughsuch abnormalities are frequently reported in patientswith BPD.1,5,21,22 Rather than presenting a decreasedslope, these BPD infants actually presented a steeperascending angle, likely due to the higher respiratoryrate.23

Abnormalities were observed on the initial inhalationphase, independent of respiratory rate, as the ratio ofinitial inhalation phase (CD) over duration of the respir-atory cycle (Ttot) was increased in BPD patient. Duringthis phase, fresh gas rinses out the CO2 from theprevious exhalation and should result in a rapiddecrease of the end-expiratory CO2.

24 An increase ofthe inhalation phase in BPD patient might be due to thedead space ventilation induced by shallow breathingand tachypnea.1

This study presents several limitations. The firstlimitation concerns the absence of actual measurementof pulmonary mechanics. The BPD infants in this seriesmay have normal pulmonary resistance due to thedifferences between so-called ‘‘old’’ BPD2 describedbefore the age of surfactant therapy, and ‘‘new’’ BPD.25

Most studies of long-term lung function have been per-formed in patients with the ‘‘old’’ form of the disease,characterized by severe bronchial and bronchiolarlesions, but only limited information is available on thepulmonary function of patients with the ‘‘new’’ form ofBPD, which mainly consists of arrested alveolar devel-opment, with less airway involvement.26 However, Hjal-marson and Sandberg,26 recently reported the absenceof increased resistances at term equivalent in patientswith BPD, supporting the hypothesis of normal resist-ances accounting for the normal expiratory capnogramphase observed in our BPD infants. Different resultswere reported in a recent prospective longitudinal studyperformed in the era of surfactant which confirmed thepresence of airflow limitations in preterm infants withBPD.6 However lung function was not evaluated at termbut from 6 months after initial discharge.

Other limitations of the study include: (i) smallgroups of infants were studied. A larger group ofpatients with varying degrees of BPD would allow moreaccurate evaluation of the expiratory and inspiratory

phases of the capnogram. (ii) Concerning the controlgroup, it would have been preferable to study controlinfants with similar gestational and chronological ageto those of the BPD group, rather than studying late-preterm infants which would have more clearly distin-guished between elements related to BPD per se andelements related to maturation. (iii) A speciallydesigned cannula was not used for simultaneous EtCO2

measurement and oxygen delivery, but two nasal cannu-las (EtCO2 cannula and air/oxygen cannula) were used,so that gas flow through one cannula may have affectedEtCO2 measured from the other cannula. We checkedthat this was not the case by comparing EtCO2 in thepresence and in the absence of the air/oxygen cannula,in five infants without lung disease. We acknowledge,however, that such small sample may not have thepower to rule out the possibility of any bias created bythe air/oxygen flow. In addition, similar comparisonswere not performed in infants with BPD.In conclusion, this study confirms the accuracy of

low-flow sidestream capnography in healthy spon-taneously breathing infants, and the existence of aPaCO2–EtCO2 gradient in infants with BPD. Wesuggest that measuring this gradient may help assesslung disease severity and exacerbations. In infants withBPD, the expiratory phase of the capnogram did notshow similar abnormalities to those reported in COPDpatients, possibly because lung resistances were notelevated in these infants. However, this remains a mat-ter of speculation in the absence of measurement ofpulmonary mechanics, in the present study. In contrast,the initial inhalation phase was longer in BPD patients,which may be due to dead space ventilation. The expir-atory phase of the capnogram, and the possible relation-ships between abnormalities of this phase and disordersof pulmonary mechanics require further investigation.

ACKNOWLEDGMENTS

The authors gratefully acknowledge the technicalassistance provided by Mr Ozenne, Deltamedics,France, and the contribution of Anthony Saul M.B.B.S,for stylistic review of the manuscript. Deltamedics,France provided technical support.

REFERENCES

1. Kinsella JP, Greenough A, Abman SH. Bronchopulmonary dys-

plasia. Lancet 2006;367:1421–1431.

2. Baraldi E, Filippone M. Chronic lung disease after premature

birth. N Engl J Med 2007;357:1946–1955.

3. Parker TA, Abman SH. The pulmonary circulation in broncho-

pulmonary dysplasia. Semin Neonatol 2003;8:51–61.

4. Mallory GB, Jr, Chaney H, Mutich RL, Motoyama EK. Longi-

tudinal changes in lung function during the first three years of

premature infants with moderate to severe bronchopulmonary

dysplasia. Pediatr Pulmonol 1991;11:8–14.



5. Parat S, Moriette G, Delaperche MF, Escourrou P, Denjean A,

Gaultier C. Long-term pulmonary functional outcome of bron-

chopulmonary dysplasia and premature birth. Pediatr Pulmonol

1995;20:289–296.

6. Fakhoury KF, Sellers C, Smith EO, Rama JA, Fan LL. Serial

measurements of lung function in a cohort of young children

with bronchopulmonary dysplasia. Pediatrics 2010;125:e1441–

e1447.

7. Krauss B, Deykin A, Lam A, Ryoo JJ, Hampton DR, Schmitt

PW, Falk JL. Capnogram shape in obstructive lung disease.

Anesth Analg 2005;100:884–888.

8. Lopez E, Grabar S, Barbier A, Krauss B, Jarreau PH, Moriette

G. Detection of carbon dioxide thresholds using low-flow side-

stream capnography in ventilated preterm infants. Intensive Care

Med 2009;35:1942–1949.

9. Ehrenkranz RA, Walsh MC, Vohr BR, Jobe AH, Wright LL,

Fanaroff AA, Wrage LA, Poole K. Validation of the National

Institutes of Health consensus definition of bronchopulmonary

dysplasia. Pediatrics 2005;116:1353–1360.

10. Colman Y, Krauss B. Microstream capnograpy technology: a

new approach to an old problem. J Clin Monit Comput 1999;

15:403–409.

11. Hagerty JJ, Kleinman ME, Zurakowski D, Lyons AC, Krauss B.

Accuracy of a new low-flow sidestream capnography technol-

ogy in newborns: a pilot study. J Perinatol 2002;22:219–225.

12. Yildizdas D, Yapicioglu H, Yilmaz HL, Sertdemir Y. Corre-

lation of simultaneously obtained capillary, venous, and arterial

blood gases of patients in a paediatric intensive care unit. Arch

Dis Child 2004;89:176–180.

13. Tirosh E, Bilker A, Bader D, Cohen A. Capnography in spon-

taneously breathing preterm and term infants. Clin Physiol

2001;21:150–154.

14. McEvedy BA, McLeod ME, Kirpalani H, Volgyesi GA, Lerman

J. End-tidal carbon dioxide measurements in critically ill neo-

nates: a comparison of side-stream and mainstream capnome-

ters. Can J Anaesth 1990;37:322–326.

15. Lucangelo U, Blanch L. Dead space. Intensive Care Med 2004;

30:576–579.

16. Scheid P, Piiper J. Blood/gas equilibrium of carbon dioxide in

lungs. A critical review. Respir Physiol 1980;39:1–31.

17. Quine D, Wong CM, Boyle EM, Jones JG, Stenson BJ. Non-

invasive measurement of reduced ventilation/perfusion ratio and

shunt in infants with bronchopulmonary dysplasia: a physiologi-

cal definition of the disease. Arch Dis Child Fetal Neonatal Ed

2006;91:F409–414.

18. Rozycki HJ, Sysyn GD, Marshall MK, Malloy R, Wiswell TE.

Mainstream end-tidal carbon dioxide monitoring in the neonatal

intensive care unit. Pediatrics 1998;101:648–653.

19. Kugelman A, Zeiger-Aginsky D, Bader D, Shoris I, Riskin A.

A novel method of distal end-tidal CO2 capnography in intu-

bated infants: comparison with arterial CO2 and with proximal

mainstream end-tidal CO2. Pediatrics 2008;122:e1219–

e1224.

20. Lujan M, Canturri E, Moreno A, Arranz M, Vigil L, Domingo

C. Capnometry in spontaneously breathing patients: the influ-

ence of chronic obstructive pulmonary disease and expiration

maneuvers. Med Sci Monit 2008;14:CR485–CR492.

21. Baraldi E, Filippone M, Trevisanuto D, Zanardo V, Zacchello F.

Pulmonary function until two years of life in infants with bron-

chopulmonary dysplasia. Am J Respir Crit Care Med 1997;155:

149–155.

22. Iles R, Edmunds AT. Prediction of early outcome in resolving

chronic lung disease of prematurity after discharge from hospi-

tal. Arch Dis Child 1996;74:304–308.

23. Thompson JE, Jaffe MB. Capnographic waveforms in the

mechanically ventilated patient. Respir Care 2005;50:100–108,

discussion 108–109.

24. Gravenstein JS, Jaffe MB, Paulus DA, editors. Capnography.

Clinical aspects. Cambridge: Cambridge University Press; 2004.

382 p.

25. Jobe AJ. The new BPD: an arrest of lung development. Pediatr

Res 1999;46:641–643.

26. Hjalmarson O, Sandberg KL. Lung function at term reflects

severity of bronchopulmonary dysplasia. J Pediatr 2005;146:

86–90.

902 Lopez et al.


capnography in spontaneously breathing preterm infants with bronchopulmonary dysplasia

Documents