Anat Cell Biol.  2018 Sep;51(3):150-157. 10.5115/acb.2018.51.3.150.

Development of the pulmonary pleura with special reference to the lung surface morphology: a study using human fetuses

• Yamamoto M
• Wilting J
• Abe H
• Murakami G
• Rodríguez-Vázquez JF
• Abe SI

• KMID: 2447007
• DOI: http://doi.org/10.5115/acb.2018.51.3.150

Abstract

In and after the third trimester, the lung surface is likely to become smooth to facilitate respiratory movements. However, there are no detailed descriptions as to when and how the lung surface becomes regular. According to our observations of 33 fetuses at 9-16 weeks of gestation (crown-rump length [CRL], 39-125 mm), the lung surface, especially its lateral (costal) surface, was comparatively rough due to rapid branching and outward growing of bronchioli at the pseudoglandular phase of lung development. The pulmonary pleura was thin and, beneath the surface mesothelium, no or little mesenchymal tissue was detectable. Veins and lymphatic vessels reached the lung surface until 9 weeks and 16 weeks, respectively. In contrast, in 8 fetuses at 26-34 weeks of gestation (CRL, 210-290 mm), the lung surface was almost smooth because, instead of bronchioli, the developing alveoli faced the external surfaces of the lung. Moreover, the submesothelial tissue became thick due to large numbers of dilated veins connected to deep intersegmental veins. CD34-positive, multilayered fibrous tissue was also evident beneath the mesothelium in these stages. The submesothelial tissue was much thicker at the basal and mediastinal surfaces compared to apical and costal surfaces. Overall, rather than by a mechanical stress from the thoracic wall and diaphragm, a smooth lung surface seemed to be established largely by the thick submesothelial tissue including veins and lymphatic vessels until 26 weeks.

Keyword

Human fetus; Lung surface; Pulmonary pleura; Mesothelium; Submesothelial morphology

MeSH Terms

Diaphragm
Epithelium
Female
Fetus*
Humans*
Lung*
Lymphatic Vessels
Pleura*
Pregnancy
Pregnancy Trimester, Third
Stress, Mechanical
Thoracic Wall
Veins

Figure

• 

  Fig. 1 Rough lung surface and pulmonary pleura at the pseudoglandular and canalicular phases. H&E staining. Sagittal sections. Panel A displays the left lung from a specimen at 9 weeks (39 mm crown-rump length [CRL]), while panels B–D exhibit the right lung from a specimen at 10 weeks (56 mm CRL). Panels C–E are higher magnification view of squares in panel B, respectively. In panel A, outward growing bronchi provide small protrusions of the lateral or costal surface (arrows). A rough surface is also evident in the costal aspect in panel B, but a mesenchymal tissue (stars) is present beneath the thin pleura (E). Deep intersegmental veins do not reach the lung surface (arrowheads in B). The canalicular phase of the bronchus was mixed with the pseudoglandular phase. upper, upper lobe; middle, middle lobe; lower, lower lobe; B6 and B8, sixth and eighth segmental bronchi; LLB, lower lobar bronchus; MLB, middle lobar bronchus; ULB, upper lobar bronchus. Scale bars=1 mm (A, B), 0.1 mm (C–E).

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  Fig. 2 Lung surface and pulmonary pleura at the saccular phase in late stage fetuses. H&E staining. Sagittal sections. Panels A and B display the left lung from a specimen at 26 weeks (215 mm crown-rump length [CRL]), while panels C and D exhibit the right lung from a specimen at 31 weeks (255 mm CRL). The subpleural tissue (stars) is thicker in the basal area than in the upper area near the apex of the lung and it contains dilated superficial veins those connected with deep, intersegmental veins. All panels were prepared at the same magnification. Scale bar=1 mm (A).

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  Fig. 3 CD34 immunohistochemistry of the lung and pleura. Sagittal sections. (A) The left lung from a specimen at 9 weeks (pseudoglandular phase; 39 mm crown-rump length [CRL]). (B) The left lung from a specimen at 15 weeks (a mixture of the pseudoglandular and canalicular phases; 115 mm CRL). (C) The left lung from a specimen at 30 weeks (saccular phase; 250 mm CRL). Panels B and D are photos of the same section and panel D displays the liver, pylorus and transverse colon. CD34 immunoreactivity is restricted in the developing vessels (arrows in A). At 15 weeks, the subpleural tissue is thin at the lung base (B), while no or little serosal tissue is seen along the liver, pylorus and colon (arrowheads in D). At 30 weeks, the subpleural tissue contains multilayered fibers expressing CD34 weakly (C). Capillaries adjacent to alveoli express CD34 strongly (arrows in C). Scale bars=1 mm.

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  Fig. 4 D2-40 immunohistochemistry of lymphatic vessels at the lung surface. (A) The right lung base from a specimen at 9 weeks (the same specimen as shown in Fig. 3A; 39 mm crown-rump length [CRL]). (B) The right lung base from a specimen at 16 weeks (a mixture of the pseudoglandular and canalicular phases; 125 mm CRL). D2-40–positive lymphatic vessels reach the lung surface until 9 weeks (arrows in A) and they are thick and abundant at 16 weeks (arrows in B). Bronchial epithelia also express reactivity of D2-40. Veins reach the lung surface at 16 weeks. Two panels were prepared at the same magnification. Scale bar=1 mm (A).

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  Fig. 5 Elastica Masson staining of the lung in late stage fetuses. Sagittal sections. Panels A and B display the left lung from a specimen at 26 weeks (215 mm crown-rump length [CRL]) and the right lung from a specimen at 31 weeks (255 mm CRL), respectively. Panel C exhibits a thick branch of the pulmonary artery from a specimen at 31 weeks (255 mm CRL). The pleura and subpleural tissue are stained dark gray (A, B), but they are different from wavy elastic fibers seen in the internal lamina of the arterial wall (C). All panels were prepared at the same magnification. Scale bar=0.1 mm (A).

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