Interstitial Syndrome And Alveolar Consolidation: Sonographic Markers of Hemodynamic Pulmonary Edema In Infants

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Abstract


With the purpose of evaluating the possibility of describing hemodynamic pulmonary edema in infants with congenital heart disease using the previously suggested sonographic phenomena “alveolar consolidation” and “interstitial syndrome” in adults, 131 children of both genders were examined at the age of 1-246 days. Of these infants, 47 had congenital heart anomalies, 51 had chronic somatic pathology and patent foramen ovale, and 33 had a somatic pathology associated with either congenital heart disease or small heart abnormalities. The duration of observation and the number of sessions of ultrasound scanning were determined by the health status dynamics of the infants. All infants were described in terms of 179 characteristics of physical examination and laboratory and instrumental findings obtained through standard procedures. Echocardiography and ultrasound lung scans were performed with LOGIQ E (General Electric) and HD11 (Philips) using linear, convex, and sector transducers (7-12, 3-5, and 1.7-4.0 МHz respectively). In addition to standard protocols of heart and lung description, we also registered the square of consolidated parcels summarized for all lung segments, the number of B-lines summarized for all lung segments, and the swing of diaphragm and lung movement and calculated the diaphragm and lung swing ratio. An attempt to describe the differences between pulmonary circulation in terms of ultrasound sonography for heart defects associated and not associated with blood filling in the lungs was successful. The total area of air-free/consolidated subpleural parcels of lungs and the extent of interstitial lung syndrome were the most informative sonographic characteristics. It was concluded that interstitial edema and alveolar consolidation, described in terms of transthoracic ultrasound sonography, are recommended for use as markers of the disorders of pulmonary circulation associated with congenital heart malformations in infants.


Background

The last decade was marked by progress in the field of diagnostics of lung diseases, particularly with the use of ultrasound imaging. The accumulation of experience in the use of transthoracic ultrasonography in the diagnostics of a sufficiently wide range of pathology attributed to the competence of internists, surgeons [10], and pediatricians [5, 19]. Moreover, special attention is paid to investigate the possibilities of employing sonography in intensive care units and newborn departments, that is, where diagnostics is required right at the patient’s bed; however, until now, these studies remain at the level of pilot projects [18, 23, 24].

Transthoracic ultrasonography of the lungs is possible because of the presence of extracellular fluid in the lung tissue. Extracellular fluid first makes the alveolar walls thicker (first phase) and then fills the alveoli (second phase) because of inflammatory or hemodynamic edema. In the first phase, the disturbance of the normal air-liquid ratio is visualized as an artifact (reverberation) that represents as linear hyperechogenic signals that can be counted and called comets [3, 4, 6, 9, 14, 15, 17] or B-lines [13, 21]. The emergence of such lines is usually considered as evidence of the so-called interstitial syndrome [12, 16, 22, 23]. During the second phase, the alveoli are filled with liquid, the pulmonary consolidation areas are visualized and counted and are called “alveolar consolidation” [11, 23].

Ultrasonography was repeatedly utilized to determine the state of the lungs in cardiac pathology in adults [7, 8, 20] than in children. This is largely because of the complex features of heart failure formation in early childhood, which in most cases makes it impossible to classify confidently.

The aim of the study is to evaluate the possibilities of using two ultrasonographic phenomena, namely, “al veolar consolidation” and “interstitial syndrome,” in detecting hemodynamic pulmonary edema in congenital heart diseases in young children.

Materials and methods

The study was conducted in the neonatal resuscitation and neonatal departments of Pediatric Department No. 3 of St. Petersburg State Pediatric Medical University.

A formalized card included 179 signs recorded during the course of physical, instrumental, and laboratory studies performed in accordance with current clinical guidelines [1, 2].

Ultrasound examination of the heart and lungs was performed using GE LOGIQ E and Philips HD11 ultrasound scanners with linear, convex, and sector probes at 7-12, 3-5, and 1.7-4.0 MHz, respectively. During the examination, the patient lay in supine position, then in prone position, and, insome cases, in the edgewise position. Diagnostic programs were expanded as part of an in-depth description of lung conditions through ultrasonography. The following sonographic characteristics of the lungs were recorded [10, 19, 24]:

  • The area of the consolidated lung sites in mm2 (AirLessTotal), total for all segments.
  • The number of B-lines in units (SDtot), total for all lung segments.
  • The amplitude of diaphragm excursion, mm (DiafMove)
  • The amplitude of lung movement, mm (LungMove)
  • The ratio of the amplitudes of the diaphragm excursion and lung movement in units, calculated value (DiafLung)

Overall, 131 pediatric patients of both genders (53% were boys) aged 1-246 days were examined. Because the present study considered the presence of any anatomical possibility of blood exchange between the small and large circulatory systems, the functioning open oval window (OOW) and open arterial duct (OAD) were considered a defect at any age. Table 1 presents the distribution of the pediatric patients examined into groups.

 

Table 1. Total number of pediatric patients examined and their distribution into the diagnosis groups

Таблица 1. Общее количество обследованных детей и их распределение по группам диагнозов

Primary diagnosis

Number of pediatric patients

Age (days)

Number of studies

Total number of the patients examined

131

1-246

240

Number of pediatric patients with congenital heart disease

47

2-246

74

Number of pediatric patients with other pathologies, including:

• other pathology + open oval window

84

51

1-130

5-97

91

76

 

The duration of observation and the number of sessions of ultrasound scanning were determined by the severity and dynamics of the child’s condition. Table 2 presents the most common characteristics of the examined patients.

 

Table 2. Brief general description of the patients examined

Таблица 2. Краткая общая характеристика обследованных

Characteristic

Mean value (M)

Average error from М

Range of values

Gestational age at birth (weeks)

33.4

0.3

24-42

Body length at birth (cm)

43.6

0.5

28-59

Body weight at birth (g)

2054

64

640-4650

Apgar 1 (points)

7 (median)

1-9

Apgar 5 (points)

7 (median)

1-9

Body weight as of the day of examination

2656

76

650-5790

 

In general, the proportion of the pediatric patients with severe condition at the start of the study was approximately 30%.

Table 3 shows the distribution of pediatric patients with cardiac pathologies according to the main diagnoses. The exclusion criteria for pediatric patients in this group are as follows: the presence of pneumonia, meconium aspiration, bronchopulmonary dysplasia, and respiratory distress syndrome.

 

Table 3. Distribution of pediatric patients with cardiac pathology according to the main diagnoses

Таблица 3. Распределение детей с патологией сердца по основным диагнозам

Defect

Age (days) at the time of examination

Number of pediatric patients

Number of studies

Dimensions (mm)

Max

Min

Only OOW

1-166

57

79

3.7

1.0

OOW in the complex

5-246

30

49

4.2

1.0

Only OAD

8-39

5

8

3.0

1.0

OAD in the complex, including:

  • Closed during the follow-up

2-104

25-97

20

2

36

7

4.5

1.0

2.0 =>

0.0

Only IASD

9-73

7

8

8.0

2.0

IASD in the complex

9-159

9

14

8.0

3.0

Only IVSD

20-124

8

9

10.0

2.0

IVSD in the complex

2-246

25

38

10.0

1.0

Pulmonary artery stenosis in the complex

10-86

3

7

Anomalous pulmonary veins drainage in the complex

2-125

2

3

Примечание: ООО — открытое овальное окно; ОАП — открытый артериальный проток; ДМПП — дефект межпредсердной перегородки; ДМЖП — дефект межжелудочковой перегородки.

Note: OOW, open oval window; OAD, open arterial duct; IASD, interatrial septal defect; IVSD, interventricular septal defect

 

In most pediatric patients, the functioning OOW, which in some cases reaches a diameter of 4.2 mm, was determined steadily with discharge of blood from left to right. However, when blood dynamics was observed, only two cases had cessation of blood flow through it.

The presented data reveals that of all the examined pediatric patients, only three had a pulmonary circuit disorder.

OAD was recorded in 53% of the pediatric patients in the cardiological group in a period of 2-104 days, and its closure was recorded in only two patients in the late period. This was because OAD was part of a combination of defects and not a single defect in most cases (see Table 4).

 

Table 4. Variants of the combinations of various defects

Таблица 4. Варианты комбинаций пороков и открытого овального окна

Defect

Age (days)

Number of pediatric patients

Number of studies

Dimensions (mm)

Max

Min

OOW

+ OAD

5-104

13

26

4.2

4.0

1.0

1.0

OOW

+ IVSD

2-246

11

15

4.0
10.0

1.0

1.0

IASD

+ IVSD

9-159

6

10

8.0

10.0

3.5

3.0

OOW

+ IVSD

+ OAD

17-61

3

7

4.0

8.0

4.5

1.0

3.0

1.5

IASD

+ OAD

77-97

1

2

8

2 => 0.0

IVSD

+ OAD

46-73

1

3

3.2

3.0

OOW

+ IVSD

+ OAD

+ anomalous pulmonary vein drainage

2

1

1

2.5

2.5

3.0

IASD

+ IVSD

+ anomalous pulmonary vein drainage

118-125

1

2

3

7 => 4

OOW

+ OAD

+ PAS

10-67

1

4

1.0

2.0

IASD

+ IVSD

+ PAS

45

1

1

5.0

3.0

OOW

+ IVSD

+ PAS

58-86

1

2

3.0

8.0

Примечание: ООО — открытое овальное окно; ОАП — открытый артериальный проток; ДМПП — дефект межпредсердной перегородки; ДМЖП — дефект межжелудочковой перегородки; СЛА — стеноз легочной артерии.

Note: OOW, open oval window; OAD, open arterial duct; IASD, interatrial septal defect; IVSD, interventricular septal defect; PAS, pulmonary artery stenosis

 

Table 5 presents the distribution of pediatric patients without heart and lung disorders. The inclusion criterion of the patients in the comparison group was the absence of history of pathology of the heart and lungs according to clinical, instrumental, and laboratory signs and absence of such pathology at the time of the study.

 

Table 5. Distribution of pediatric patients without heart and lung diseases by diagnoses

Таблица 5. Распределение детей без поражения сердца и легких по диагнозам

Diagnosis

Number of the patients examined

Age (days) at the time of examination

Number of studies

Intra-amniotic infection of the fetus

31

2-97

40

Hypoxic injury of the CNS

32

1-130

51

Diseases of the GIT, moderate hypotrophy

21

1-166

23

Примечание: ЦНС — центральная нервная система; ЖКТ — желудочно-кишечный тракт

Note: CNS, central nervous system; GIT, gastrointestinal tract

 

Due to the multifactor data of the phenomena under study, multiple regression analysis and routine parametric estimation methods (Student–Fischer t-test) were used to analyze obtained results. The data was statistically analyzed by the standard tools of Statistica for Windows ver. 6 (StatSoft Inc., No. AX204B521115F60).

Results

An attempt to describe the hemodynamics of the pulmonary circuit with defects are priori known to affect (incomplete drainage of the pulmonary veins) and do not affect (OOW) the filling of the pulmonary circuit through ultrasonography appeared to be successful (see Table 6). Furthermore, no differences were observed between groups of pediatric patients with and without a functioning oval window on the basis of the registered characteristics, despite the fact that the size of the window in a significant proportion of the children was quite large (see Table 3). In incomplete drainage of the pulmonary veins, there was a significant 3.8 times increase in the area of alveolar consolidation (AirLessTotal) (p = 0.045), with no differences in the size of the left atrium, right ventricle, pulmonary artery diameter, blood peak flow, and mean pulmonary artery pressure due to the presence of compensating defects.

 

Table 6. Significance of the characteristics describing interstitial syndrome and alveolar consolidation and pulmonary heart in pediatric patients with an OOW and incomplete drainage of pulmonary veins through ultrasonography

Таблица 6. Значение характеристик, описывающих интерстициальный синдром и альвеолярную консолидацию, а также характеристик правых отделов сердца в терминах ультразвуковой сонографии у детей с открытым овальным окном и неполным дренажом легочных вен

Defect type

Characteristic

Mean value

T

p

0*

1*

OOW without other defects

AirlessTotal

96.88000

64.97468

1.15164

0.250829

SDtot

10.70400

9.94937

0.77272

0.440593

LA

10.53660

10.57568

–0.10054

0.920032

RV

9.71099

10.10000

–0.64921

0.517238

PA

7.90408

8.55541

–1.02932

0.304793

PAVmax

1.30029

1.13615

1.06965

0.286201

PAP

25.77027

23.11087

1.18104

0.239960

Incomplete drainage of pulmonary veins combined with other defects

AirlessTotal

78.44000

299.0000

–2.02040

0.044669

SDtot

10.40000

13.0000

–0.65700

0.511934

LA

10.53472

12.1500

–0.88738

0.376072

RV

9.84056

10.6667

–0.40327

0.687348

PA

8.18343

8.2333

–0.02079

0.983440

PAVmax

1.22556

1.5167

–0.48593

0.627602

PAP

24.90254

15.8000

1.06322

0.289851

Примечание: 0* — нет дефекта, 1* — есть дефект, выделено существенное различие; LA — диаметр левого предсердия (мм); RV — диаметр правого желудочка (мм); PA — диаметр легочной артерии (мм); PAVmax — максимальная скорость кровотока в легочной артерии (м/с); PAP — среднее давление в легочной артерии (мм Hg).

Note: 0*, no defect; 1*, presence of a defect, an essential difference is allocated; LA, diameter of the left atrium (mm); RV, diameter of the right ventricle (mm); PA, diameter of the pulmonary artery (mm); PAV, blood peak flow in the pulmonary artery (m/s); PAP, average pressure in the pulmonary artery (mm Hg); OOW, open oval window

 

Considering that the sample had a large number of complex defects, multiple linear regression modeling (stepwise inclusion) was performed, with a preliminary choice of factors at the level of interconnection not exceeding 0.4. A total of 19 models were created with explained dispersion level of 35%-82% with the included characteristics, namely, AirLessTotal, SDtot, LungMove, and DiafMove, treated in combination and individually. Tables 7 and 8 show the results of the modeling using SDtot and RV characteristics, control, physical, and laboratory characteristics, as well as characteristics of the heart and right lung segment in terms of ultrasonography. The regression of coefficients equation presented in Table 7, which shows an insignificant correlation of the characteristics (Durbin–Watson correlation coefficient of 0.26), provide 78% of the explained dispersion of the SDtot characteristic value, thereby reflecting the severity of the interstitial syndrome.

 

Table 7. Results of the regression modeling of the SDtot characteristic value. Regression summary for dependent variable: SDtot (ivan_data_w9), R = 0.93244324, R = .93244324 R2 = .86945039 Adjusted R2 = .76263707 F(9,11) = 8.1399 p < .00099 Std. Error of estimate: 2.4241 Durbin-Watson d =1.472474, Serial Corr. 0.263094

Таблица 7. Результаты регрессионного моделирования значения характеристики SDtot. Regression Summary for Dependent Variable: SDtot (ivan_data_w9), R = .93244324 R2 = .86945039 Adjusted R2 = .76263707 F(9,11) = 8.1399 p < .00099 Std. Error of estimate: 2.4241 Durbin-Watson d =1.472474, Serial Corr. 0.263094

Characteristics studied

BETA

Std. Err.

of BETA

B

Std. Err.

of BETA

p-level

Intercept

  

100.0492

19.64767

0.000348

m

–0.856598

0.259351

–0.0041

0.00125

0.007042

CardRate

–0.992885

0.167861

–0.6257

0.10579

0.000101

AirLessTotal

0.316251

0.130543

0.0523

0.02160

0.033851

PAVmax

–0.237113

0.130261

–7.3759

4.05203

0.096003

pO2

–0.107595

0.141044

–0.0469

0.06149

0.461603

PA

–0.659042

0.233702

–2.9361

1.04117

0.016667

RespRate

0.405810

0.161775

0.6498

0.25902

0.029065

DiafLung

0.280194

0.133050

2.0494

0.97313

0.058991

mass

0.425926

0.321814

0.0022

0.00163

0.212513

Примечание: m — масса тела при рождении (г); CardRate — частота сердечных сокращений в момент исследования (1/мин); pO2 — напряжение кислорода в плазме крови в момент исследования (мм Hg); RespRate — частота дыханий в момент исследования (1/мин); mass — масса тела в момент исследования (г); прочие обозначения — см. пояснения к табл. 6 и в тексте, выделены существенные значения.

Note: m, birth weight (g); CardRate, the heart rate at the time of the study (1/min); PO, oxygen tension in blood plasma at the time of the study (mm Hg); RespRate, respiration rate at the time of the study (1/min); mass, body mass at the time of the study (d); other designations, see the explanations to Table 6 and in the text; the significant values are highlighted

 

The negative coefficients with statistically significant characteristics for m, CardRate, and PA, which indicate that the SDtot value is greater in pediatric patients born with a low body weight and who have bradycardia with a small pulmonary artery diameter at the time of examination, is of particular interest. Together with the positive coefficients for the AirLessTotal and RespRate characteristics, the model correctly describes the known fundamental regularities, and the coefficient values indicate that pulmonary artery diameter greatly contributed to the formation of the interstitial syndrome compared to the birth weight.

Table 8 presents the coefficients of the characteristics of the regression equation that determines the size of the right ventricle. In accordance with classical notions of physiology, it was assumed that the interstitial syndrome and alveolar consolidation, with their sufficient severity and duration,affect the size of the right ventricle on a par with, for example, the effect of the size of the septal defects. The coefficients of the regression equation presented in Table 8, with a moderate interrelation of characteristics (Durbin–Watson correlation coefficient of 0.37) indicated 42% of the explained dispersion of the RV characteristic value.

 

Table 8. Results of the regression modeling of the RV characteristic value. Regression summary for dependent variable: RV (ivan_data_w9) R = .69223739 R2 = .47919260 Adjusted R2 = .41932968 F(10,87) = 8.0048 p < .00000 Std. Error of estimate: 2.1761 Durbin-Watson d = 1.263156, Serial Corr. 0.3680869

Таблица 8. Результаты регрессионного моделирования значения характеристики RV. Regression Summary for Dependent Variable: RV (ivan_data_w9) R = .69223739 R2 = .47919260 Adjusted R2 = .41932968 F(10,87) = 8.0048 p < .00000 Std. Error of estimate: 2.1761 Durbin-Watson d = 1.263156, Serial Corr. 0.3680869

Исследуемые характеристики

BETA

Std. Err.

of BETA

B

Std. Err.

of BETA

p-level

Intercept

  

1.230303

1.595912

0.442850

M

0.238464

0.099291

0.000708

0.000295

0.018449

PAP

0.312879

0.085093

0.093431

0.025410

0.000408

LA

0.272323

0.094498

0.300839

0.104394

0.004980

SDtot

0.316294

0.105903

0.146247

0.048967

0.003664

OAD

–0.200700

0.084468

–0.618692

0.260388

0.019695

OOO

0.245074

0.086941

0.572891

0.203234

0.005966

DMPP

0.189365

0.089900

0.430067

0.204173

0.038051

PA

–0.158417

0.080136

–0.087918

0.044474

0.050225

AirLessTotal

–0.202964

0.099895

–0.003599

0.001771

0.045227

Days

0.167797

0.092230

0.013347

0.007337

0.072302

Примечание: OAD — диаметр функционирующего артериального протока (мм); ООО — диаметр функционирующего овального окна в комплексе дефектов (мм); DMPP — диаметр дефекта межпредсердной перегородки (мм); Days — день жизни на момент обследования; прочие обозначения — см. пояснения к табл. 6, 7 и в тексте, выделены существенные значения.

Note: OAD, diameter of the functioning arterial duct (mm); OOO, diameter of the functioning oval window in the complex of defects (mm); DMPP, diameter of interatrial septal defect (mm); Days, the day of life at the time of the examination; other designations, see the explanations in Tables 6 and 7 and in the text; the significant values are highlighted

 

Apparently, ultrasonographic characteristics reflecting the interstitial syndrome and alveolar consolidation reliably determine the size of the right ventricle.

The negative coefficient for the OAD characteristic is explained by the fact that a significant number of OAD, such as 7 of 12 without taking into account the complex with an OOW (see Table 4), were involved in complex defects for which a decrease in the discharge along the duct leads to an increase in blood flow in another defect. This also explains the effect of the diameter of the oval window. The negative coefficient in the PA characteristic is natural, and the negative coefficient in the AirLessTotal characteristic has no explanation and requires additional study using detailed measurement of the pressures within the cardiac chambers.

Discussion

Our results confirm the expediency of using the descriptions of interstitial syndrome and alveolar consolidation in terms of ultrasonography to assess the severity of hemodynamic pulmonary edema in young children.

The frequency of inclusion of SDtot and AirLessTotal characteristics in regression models that describe the state of children’s lungs with congenital heart diseases through indirect signs is extremely high.

SDtot (more often) and AirLessTotal (less often) characteristics were included in almost all models, and the results of the modeling almost always corresponded to the classical notions of clinical physiology in describing the hemodynamics of the pulmonary circuit. The rare inclusion of DiafMove, LungMove, and DiafLung characteristics in the models was somewhat surprising, which can be partly explained by the low extensibility of the lungs at this age and the fact that the diaphragm is of less importance in organizing external respiration in infants.

The rarer inclusion of the AirLessTotal characteristic can be explained by technical difficulties in calculating the consolidation area, which resulted in a larger error, as well as by the small number of pediatric patients with consolidation, because the number of pediatric patients with the firstphase of edema at such an early age significantly exceeds the number of pediatric patients with a second phase of edema.

The disadvantage of the model, which equation is presented in Table 7, is that it includes all control characteristics, with the exception of body weight and, in a less degree, the diameter of the pulmonary artery, and the period of variability in time is minutes/hours. At the same time, the period of change in the pronouncement of the controlled variable, which is the interstitial syndrome, is much longer (in days). This implies a high proportion of randomness in obtaining the values of the coefficients in such a combination. The model, which characteristics and coefficients of the equation are presented in Table 8, partly eliminates this disadvantage because the variability period of controlled and controlling variables are approximated to comparable quantities.

Conclusions

  1. Interstitial edema and alveolar consolidation, described in terms of transthoracic ultrasonography, should be used as markers of hemodynamic disorders of the pulmonary circuit in congenital malformations in children at an early age.
  2. The characteristics of interstitial edema and alveolar consolidation are reliably associated with clinical, laboratory, and instrumental signs of the pulmonary circuit.

Therefore, additional studies are required to develop the decisive rules for differential diagnostics of various types and stages of hemodynamic disorders of the pulmonary circuit and to determine diagnostic errors when using transthoracic ultrasonography as well as the measurement of pressures within the heart cavities and large vessels.

Ahlam A. Mohammad

Author for correspondence.
d.ahlam@mail.ru
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

Postgraduate Student, Department of Hospital Pediatrics

Ivan I. Akinshin

akinshinivan87@gmail.com
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

Postgraduate Student, Department of Radiology and Biomedical Imaging Faculty of Postgraduate Education

Elena V. Sinelnikova

sinelnikavae@gmail.com
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

MD, PhD, Dr Med Sci, Professor, Head, Department of Radiology and Biomedical Imaging Faculty of Postgraduate Education

Alla J. Rotar

a_lepenchuk@mail.ru
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

Student, Department of Radiology and Biomedical Imaging Faculty of Postgraduate Education

Vyacheslav G. Chasnyk

chasnyk@gmail.com
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

MD, PhD, Dr Med Sci, Professor, Head, Department of Hospital Pediatrics

Irina V. Solodkova

isolodkova@mail.ru
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

MD, Associate professor, Chair of Hospital Pediatrics

Elena V. Baryshek

barishek@yandex.ru
St Petersburg State Pediatric Medical University
Russian Federation, Saint Petersburg

MD, Professor, Chair of Hospital Pediatrics

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