Congenital diaphragmatic hernia

Respiratory Repercussions

Objective: Diaphragmatic reconstruction may cause several respiratory changes. The aims of the present study were to evaluate the respiratory changes induced by two methods of diaphragmatic reconstruction.

Methods: Two groups of rats with an experimental diaphragmatic defect were studied. In one group (n = 5), diaphragmatic resection was followed by stitching together the borders of the wound (SUT); in another group (n = 5), the defect was repaired by suturing in a polytetrafluoroethylene (PTFE) patch. All animals were sedated, anesthetized, paralyzed, and mechanically ventilated. Spirometry, respiratory mechanics, and thoracoabdominal morphometry were evaluated before and after diaphragmatic reconstruction.

Results: The suture of the diaphragm significantly decreased FVC and [FEV.sub.1], and increased respiratory system, lung, and chest wall static and dynamic elastances and viscoelastic/inhomogeneous pressures in relation to their respective control values. On the other hand, diaphragmatic reconstruction with PTFE increased only respiratory system, lung, and chest wall static elastances. In addition, respiratory system, pulmonary, and chest wall viscoelastic/inhomogeneous pressures and dynamic elastances, as well as respiratory system and lung elastances, were significantly greater in SUT than in PTFE. Lateral diameter at the level of the xiphoid and cephalocaudal pulmonary diameter diminished only in the SUT group.

Conclusions: The reconstruction of the diaphragm with PTFE might be preferred to simple suture for surgical repair of large diaphragmatic defects, at least from a mechanical standpoint.

(CHEST 2000; 117:1443-1448)

Key words: diaphragm; elastance; mechanical inhomogeneities; prosthetic materials; viscoelasticity

Abbreviations: Dcc = pulmonary cephalocaudal diameter; [Delta]E = difference between dynamic and static elastances; Edyn = dynamic elastance; Est = static elastance; L = lung; [Delta][P.sub.1] = resistive pressure change; [Delta][P.sub.2] = viscoelastic/ inhomogeneous pressure change; Pel = elastic recoil pressure; PTFE = polytetrafluoroethylene; [Delta]Ptot = total change in pressure after airway occlusion at end inspiration; Ptr = tracheal pressure; RS = respiratory system; SUT = suture alone experimental group; V = volume; V = flow; VT = tidal volume; W = chest wall

The correction of diaphragmatic defects resulting from trauma, congenital diaphragmatic hernia, or agenesis remains a complex surgical problem. The technique to be used depends on several factors, among which the size of the defect seems to be the most important.[1,2] The goals of the various corrective procedures are restoration of adequate ventilatory dynamics and protection of the lung. Although many surgeons prefer to repair the defect by suturing together the remaining diaphragmatic borders, occasionally primary closure may be impossible, and synthetic materials have been commonly used to replace the absent diaphragm. Among the most widely used materials for diaphragm replacement and reinforcement is polytetrafluoroethylene (PTFE). Although this surgery is frequently performed, no comprehensive analysis of respiratory mechanical changes associated with diaphragmatic suture or prosthetic reconstruction with PTFE has been previously reported. Thus, the present investigation was designed to: (1) study spirometric variables; (2) compute respiratory system, lung, and chest wall resistive, elastic, and viscoelastic/ inhomogeneous mechanical components; and (3) correlate the mechanical findings with measurements of thoracoabdominal morphometry after diaphragmatic suture or prosthetic reconstruction with PTFE. In addition, the results provided by both surgical approaches were compared.

Therefore, in the present study, respiratory mechanics were evaluated by means of sudden airway occlusions at end-inspiration under constant flow inflation of the lungs.[3-5] This method provides a means of obtaining elastic and resistive pressure changes. It also provides another quantity, viscoelastic and/or inhomogeneous pressure, that can be closely related to stress relaxation (or stress recovery) properties of the lung and chest wall tissues, together with a tiny contribution of pendelluft in normal situations[3,6,7] and asynchrony of movement within and between chest wall components.[8,9]

MATERIALS AND METHODS

An experimental diaphragmatic defect was performed in two sets of male Wistar rats. In the suture (SUT) group (n = 5), the diaphragmatic defect was repaired by stitching together the borders of the wound. In the PTFE group (n = 5), a prosthetic patch of expanded PTFE was sutured. The body weight range was 240 to 250 g (246 [+ or -] 4.1 g [mean [+ or -] SD]). The animals were sedated (diazepam, 5 mg intraperitoneally) and anesthetized (pentobarbital sodium, 20 mg/kg intraperitoneally), and a snug-fitting cannula (1.7 mm internal diameter) was introduced into the trachea. They were then placed in the supine position on a surgical table.

An adequate pneumotachograph[10] was connected to the tracheal cannula for the measurements of airflow (V) and changes in lung volume (VT). The pressure gradient across the pneumotachograph was determined by means of a Validyne MP 45-2 differential pressure transducer (Northridge, CA). The flow resistance of the equipment (Req), tracheal cannula included, was constant up to flow rates of 26 mL/s, and amounted to 0.092 cm [H.sub.2]O [multiplied by] s [multiplied by] [mL.sup.-1]. Equipment resistive pressure (Req [multiplied by] V) was subtracted from respiratory system and pulmonary resistive pressures, so that the present results represent intrinsic values. Because abrupt changes of diameter were not present in our circuit, errors of measurement of flow resistance were probably avoided.[11,12] The equipment dead space was 0.4 mL. Tracheal pressure (Ptr) was measured with a Validyne MP45-2 differential pressure transducer. Changes in esophageal pressure, which reflects chest wall pressure (PW), were measured with a 30-cm-long water-filled catheter (PE-240), with side holes at the tip, connected to a PR23-2D-300 Statham differential pressure transducer (Hato Rey, Puerto Rico). The catheter was passed into the stomach, and then slowly returned into the esophagus; its proper positioning was assessed using the "occlusion test."[13]

Muscle relaxation was achieved with gallamine triethiodide (2 mg/kg IV), and artificial ventilation was provided by a Salziner constant-flow ventilator (Instituto do Coracao-USP; Sao Paulo, SP, Brazil). During the test breaths, a 5-s end-inspiratory pause could be generated, whereas during the baseline ventilation no pause was used. To avoid the effects of different flows and volumes[14,15] and inspiratory duration[4] on the measured variables, special care was taken to keep VT (1.5 mL) and V (8 mL/s) constant in all animals.

The frequency responses of the pressure measurement system (Ptr and esophageal pressure) were flat up to 20 Hz, without appreciable phase shift between the signals. All signals were conditioned and amplified in a Beckman type R Dynograph (Schiller Park, IL). Flow and pressure signals were also passed through eight-pole Bessel filters (902LPF; Frequency Devices; Haverhill, MA) with the corner frequency set at 100 Hz, sampled at 200 Hz with a 12-bit analog-to-digital converter (DT2801A; Data Translation; Marlboro, MA), and stored on a PC-compatible computer. All data were collected using LABDAT software (RHT-InfoDat; Montreal, Quebec, Canada).

The animals underwent longitudinal laparotomy. A 5-cm midline skin incision was made to the linea alba. Then a left subcostal incision was performed, and the hemidiaphragm was exposed. In this condition, the respiratory measurements were performed while the abdomen remained open (control subjects). Right before the pleural cavity was entered, a positive end-expiratory pressure of 2 cm [H.sub.2]O was applied. In both groups, a defect was created by excising a 1.5- x 0.5-cm muscular segment of the left costal diaphragm, the tendinous center remaining untouched. The resection area was kept constant, centered both anteroposteriorly (longer length) and between the central tendon and the costal border, and corresponded to approximately 20% of the total muscular area of the left hemidiaphragm in a 250-g rat. In the SUT group, the defect was repaired without tension by suturing the borders of the diaphragm with 5-0 running polypropylene suture. In the PTFE group, the diaphragm was reconstructed by implanting a 2.0- x 2.0-cm patch of PTFE with 5-0 running polypropylene suture, placed 2 mm from the edge of the defect. The patch was tailored so that normal diaphragm contours were reconstituted while minimal tension was placed on the repair. In addition, a catheter (1.5 mm external diameter) was inserted into the pleural cavity at the level of the seventh intercostal space. For this purpose, the catheter was assembled inside a needle, the distal extremity of which was air tight. After the introduction of the needle tip into the thoracic cavity, a catheter segment of about 2 cm was then inserted, and the needle was removed. The catheter was secured in place, and the air tightness was assured by stitching the skin around the catheter. This chest catheter was connected to a water seal apparatus, and suction was periodically applied with a 20-mL syringe. To eliminate the pneumothorax, in all instances the last stitch was applied to the diaphragm while the lungs were kept inflated to total lung capacity (Ptr, +30 cm [H.sub.2]O). Right after chest wall closure, the lungs underwent radioscopic examination in an attempt to identify the presence of pneumothorax or any other undesirable alteration. Spirometry, respiratory mechanics, and thoracoabdominal morphometry were studied before surgery (control subjects) and immediately after diaphragmatic closure with suture or prosthesis. The experiments did not last more than 90 min.

Spirometry: The forced expiration method[16] was performed six to eight times in each animal to obtain spirometric variables. Briefly, the lungs were inflated to a Ptr of 30 cm [H.sub.2]O, and after a 5-s inspiratory pause, a negative pressure of -30 cm [H.sub.2]O was applied to the airway, thus producing an FVC maneuver. Off-line processing produced flow and volume tracings, generating the following variables: FVC, peak expiratory flow, forced expiratory flow from 25% to 75% of FVC, and [FEV.sub.1].

Respiratory mechanics: Respiratory mechanics were measured with the end-inflation occlusion method.[3,4,14] After end-inspiratory occlusion, there is an initial fast drop in tracheal pressure ([Delta][P.sub.1]RS) from the preocclusion value down to an inflection point (PiRS). A slow pressure decay ([Delta][P.sub.2]RS) ensues until a plateau is reached (elastic recoil pressure of the respiratory system, PelRS). The same procedures apply to the chest wall pressure (PW), yielding the values of [Delta][P.sub.1]W, PiW, [Delta][P.sub.2]W, and PelW, respectively. Transpulmonary pressures ([Delta][P.sub.1]L, PiL, [Delta][P.sub.2]L, and PelL) were calculated by subtracting the chest wall data from the corresponding values pertaining to the respiratory, system. Total pressure drop ([Delta]Ptot) is equal to the sum of [Delta][P.sub.1] and [Delta][P.sub.2], yielding the values of [Delta]PtotRS, [Delta]PtotL, and [Delta]PtotW. Respiratory system, lung, and chest wall static elastances (EstRS, EstL, and EstW, respectively) were calculated by dividing PelRS, PelL, and PelW, respectively, by VT. Dynamic elastances of the respiratory system, lung, and chest wall (EdynRS, EdynL, and EdynW, respectively) were obtained by dividing PiRS, PiL, and PiW, respectively, by VT. [Delta]E was calculated as the difference between Edyn and Est, yielding the values of [Delta]ERS, [Delta]EL, and [Delta]EW. The data concerning respiratory system, lung, and chest wall elastances were presented in terms of Est and [Delta]E instead of Edyn because the former represent, respectively, the elastic and viscoelastic properties of the respiratory system.[4] In all instances, respiratory mechanics measurements were performed six to eight times in each animal in each condition.

Pressure-volume curves were performed by changing the lung volume with a calibrated syringe (0.5-mL steps up to 3 mL) and recording the corresponding pressure at each equilibrium point (5 s after injection).

Immediately before each maneuver, the airways were aspirated to remove possible mucus collection, and the respiratory system was inflated three times to total lung capacity to keep volume history constant.

All data were analyzed using ANADAT data analysis software (RHT-InfoDat Inc).

Morphometry: Chest wall conformational changes were determined in another six Wistar rats (250 [+ or -] 10 g; range, 240 to 250 g): three belonging to the SUT group and three to the PTFE group ventilated and prepared as described above. Lateral diameters at the third intercostal space and xiphoid levels, and pulmonary cephalocaudal diameter (Dcc) were measured before and after diaphragmatic reconstruction. Diameters were directly obtained with a caliper. Dcc, the distance from the lung apex to the diaphragmatic dome, was determined as follows: two needle shafts were transversally introduced through the rat skin at 90 [degrees] relative to the body length at the third intercostal space and xiphoid levels to correct for radiographic size magnification. Under radioscopic examination, two lengths were measured on the monitor: (1) between the two needle shafts, and (2) the lung apex-diaphragmatic dome distance. Because the space between the two needles was measured in the rats with a caliper and the display was linear, Dec could be easily calculated.[17] The angle between the costal fibers of the left diaphragm and the rib cage was measured under radioscopic examination with a goniometer. The measurements were performed three times by the same investigator in each animal at functional residual capacity, under the same circumstances as described for spirometry and respiratory mechanics analysis (above). Special care was taken to make the measurements at the same reference points and to avoid errors related to soft tissue compressibility.

All animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide for the Care and Use of Laboratory Animals" prepared by the National Academy of Sciences.

Statistical analysis was performed by means of Student's paired t test when the data gathered after surgery were compared with their respective control values. To compare the results between the two experimental groups, Student's t test was used. The significance level was always set at 5%.

RESULTS

Spirometric variables are shown in Figure 1. The reconstruction of the diaphragmatic defect by stitching the borders together (SUT) lead to a significant decrease in FVC and [FEV.sub.1], although forced expiratory flow from 25% to 75% of FVC and peak expiratory flow remained unaltered. However, when a patch of PTFE was used to repair the defect, no spirometric changes could be detected. In addition, FVC and [FEV.sub.1] presented significantly greater values in the PTFE group than in the SUT group (16% and 17%, respectively).

[Figure 1 ILLUSTRATION OMITTED]

The mean constant inspiratory flows ([+ or -] SEM) measured before and after surgery were 8.4 [+ or -] 0.1 and 8.2 [+ or -] 0.1 mL/s (SUT) and 8.2 [+ or -] 0.1 and 8.4 [+ or -] 0.2 mL/s (PTFE), respectively. The corresponding tidal volumes were: 1.5 [+ or -] 0.01 and 1.5 [+ or -] 0.02 mL (SUT) and 1.5 [+ or -] 0.02 and 1.5 [+ or -] 0.03 mL (PTFE). No statistically significant differences within and between the groups could be detected.

Figure 2 shows the mean values (+ SEM) of [Delta]PRS, [Delta]PL, and [Delta]PW obtained before (CTRL) and right after surgery in the two groups of animals. In the SUT group [Delta]PtotRS, [Delta]PtotL, and [Delta]PtotW were significantly increased because of augmented [Delta][P.sub.2]RS, [Delta][P.sub.2]L, and [Delta][P.sub.2]W, respectively. However, reconstruction of the diaphragm with PTFE yielded no changes in [Delta]P. In addition, [Delta]PtotRS, [Delta]PtotL, [Delta][P.sub.2]RS, [Delta][P.sub.2]L, and [Delta][P.sub.2]W presented significantly greater values in the SUT group than in the PTFE one (23%, 32%, 40%, 40%, and 38%, respectively).

[Figure 2 ILLUSTRATION OMITTED]

Figure 3 shows Est and [Delta]E obtained before (control) and right after surgery in the two groups of rats. EstRS, EstL, and EstW increased significantly in the SUT and PTFE groups. The reconstruction of the diaphragm with PTFE prosthesis resulted in smaller EstRS and EstL than in the SUT group. These data were supported by pressure-volume curves (Fig 4). EstW increased similarly in both groups. [Delta]ERS, [Delta]EL, and [Delta]EW were augmented only in the SUT group and presented significantly greater values in the SUT group than in the PTFE one.

[Figures 3-4 ILLUSTRATION OMITTED]

Table 1 shows thoracic configuration data measured before and after surgery at functional residual capacity. Lateral diameter at the xiphoid level and Dcc decreased significantly after suturing diaphragmatic borders. The angle between the costal fibers of the left diaphragm and the rib cage increased significantly in both groups and differed significantly between themselves.

(*) Data are means ([+ or -] SEM) of six animals (three measurements/rat). Dlic and Dlx = rib cage lateral diameters at the third intercostal space and xiphoid levels, respectively; Angle = angle between left diaphragm and rib cage; CTRL.S and CTRL.P = CTRL groups before SUT and PTFE patching, respectively.

([dagger]) Data significantly different from their respective CTRL values (p < 0.05).

([double dagger]) Values significantly different between SUT and PTFE groups (p < 0.05).

DISCUSSION

The diaphragm reconstruction technique depends on several factors, among which the cause and size of the defect seem to be the most important. Most diaphragmatic hernias can be repaired by primary closure. However, when the defect is large or there is tension on the closure, the use of a prosthetic material is indicated.[18] The goals of the various procedures applied are restoration of adequate ventilatory dynamics and protection of intrathoracic organs.

The use of prosthetic material has earned praise for providing better stability with shorter and simpler procedures. PTFE is among the materials used for diaphragm replacement.

In the present work, the prosthesis was not superimposed on diaphragmatic tissues. In accordance with previous studies,[19] the prosthetic material was sutured to be drum tight without excessive tension. In all instances, postmortem inspection revealed an undamaged suture line.

When V and VT remain constant, changes in [Delta]PtotRS reflect modification of respiratory system resistance, viscoelasticity, and/or inhomogeneity. [Delta]PtotRS, [Delta]PtotL, and [Delta]PtotW increased only in the SUT group (Fig 2).

It has been demonstrated in cats,[14] dogs,[3] rats,[20] and humans[15] that changes in [Delta][P.sub.1]L, when V and VT remain constant, reflect pressure losses against frictional resistances, and [Delta][P.sub.1]W corresponds to the pressure necessary to overcome chest wall tissue viscous forces.[4,14] In both groups, surgery did not induce any significant change in the pressures used to overcome lung and chest wall resistances.

Variations in [Delta][P.sub.2]RS can be closely related to stress relaxation properties of lung and chest wall tissues, together with a tiny contribution of pendelluft and asynchrony of movement within and between the chest wall components.[6,20] In other words, [Delta][P.sub.2]RS can reflect pressure losses caused by viscoelastic properties and/or mechanical inhomogeneities of lung and chest wall. In the SUT group, there was a significant increase in [Delta][P.sub.2]RS secondary to a rise in lung and chest wall viscoelastic properties. These findings could also be ascribed to conformational changes of the chest wall, which was modified after suturing the borders of the diaphragm (Table 1).

In both groups EstL, and EstW lead to increased EstRS (Fig 3), thus indicating that the elastic component of the respiratory mechanical profile was augmented under these experimental conditions. The increase in EstL in the SUT group could be attributed to pulmonary base microatelectasis caused by the significant reduction in the left lung Dcc (from 2.8 to 2.5 cm). This fact can explain the reduction of FVC and [FEV.sub.1]. It is important to note that these spirometric alterations did not occur in the PTFE group, in which modifications in the Dcc were not significant (from 2.8 to 2.7 cm). The considerable increase in the angle formed by the left hemidiaphragm with the lateral rib cage, verified in the SUT group (Table 1), may have contributed to the increase of EstW as well as to the reduction of the lung volumes. An EstW increase can be generated by diaphragmatic stretching as well as by conformational alterations of the chest wall. The reduction in diaphragmatic area causes the last ribs to cave in, diminishing the lower rib cage dimensions. These changes were observed through the measurement of the lateral diameter at the level of the xiphoid, which diminished only in the SUT group. These findings match the work of Augusto et al,[21] who analyzed the effect of progressive intraperitoneal effusions on respiratory mechanics and demonstrated that conformational modifications of the diaphragm and reduction of Dcc were responsible for the significant increase of the Est.

EstW in the PTFE group was higher than its control group, but was not different from EstW in the SUT group. Because the chest wail conformational alterations of the PTFE group were not significant, the increase in EstW could be related to the fact that in paralyzed patients, ventilation occurs preferentially in the nondependent zones of the lung.[22] A material with minute compliance (PTFE) placed in this region of the diaphragm could possibly raise EstW.

In conclusion, although both diaphragmatic SUT and PTFE patching mechanically change the respiratory system, the latter seems to assure less important respiratory dysfunction. Hence, in a clinical situation in which either technique could be used, bearing in mind the mechanical point of view, the surgeon might decide for the PTFE patch. Clearly, the direct application of the present findings to human beings is unwarranted, but they indicate an unequivocal trend that should be pursued in further clinical experiments.

ACKNOWLEDGMENT: The authors thank Antonio Carlos de Souza Quaresma for skillful technical assistance.

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[17] Sousa AS, Moll RJ, Pontes CF, et al. Mechanical and morphometrical changes in progressive bilateral pneumothorax and pleural effusion in normal rats. Eur Respir J 1995; 8:99-104

[18] Bauer JJ, Salky BA, Gelernt IM, et al. Repair of large abdominal wall defects with expanded polytetrafluoroethylene (PTFE). Ann Surg 1987; 206:765-769

[19] Macedo-Neto AV, Santos LV, Menezes SLS, et al. Respiratory mechanics after prosthetic reconstruction of the chest wall in normal rats. Chest 1998; 113:1667-1672

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(*) From the Laboratory of Respiration Physiology, Carlos Chagas Filho Biophysics Institute, Federal University of Rio de Janeiro, Ilha do Fundao, 21949-900, Rio de Janeiro, RJ, Brazil. Supported by Centers of Excellence Program (PRONEX-MCT), Brazilian Council for Scientific and Technological Development (CNPq), and Financing for Studies and Projects (FINEP). Manuscript received February 5, 1999; revision accepted November 5, 1999.

Correspondence to: Walter A. Zin, MD, PhD, Universidade Federal do Rio de Janeiro, Centro de Ciencias da Saude, Instituto de Biofisica Carlos Chagas Filho, Ilha do Fundao, 21949-900, Rio de Janeiro, RJ, Brazil; e-mail: wazin@biof.ufrj.br

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