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Respiration Physiology 109 (1997) 177194

The elephants respiratory system: adaptations to gravitationalstress

R.E. Brown a,c, J .P. Butler a, J .J . Godleski a, S.H. Loringa,b,*

a Physiology Program, School of Public H ealth, H arard Uniersity, Boston, M A 02115, U SAb Department of Anesthesia, D A 717, Beth I srael D eaconess M edical Center, Boston, M A 02215, U SA

c Zoological Institute, Depart ment of Z oomorphology, Gotebor g U niersity, M edicinaregatan 18, S-413 90Gotebor g, Sweden

Received 13 M ay 1997; received in revised form 22 M ay 1997; accepted 22 M ay 1997

Abstract

Elephants have had to adapt to gravitational stresses imposed on their very large respiratory structures. Wdescribe some unusual features of the elephants respiratory system and speculate on their functional significance.

distensible network of collagen fibers fills the pleural space, loosely connects lung to chest wall but appears not tconstrain lung-chest wall movements. M yriad spaces within the network and its rich supply of capillaries sugge

effective local sources and sinks for pleural fluid that may replace the gravity-dependent flows of smaller mammaThelung is partitioned into 1 cm3 parenchymal units by a system of thick, elastic septa that ramify throughout thlung from origins on the lungs elastic external capsule. Parenchymal units suspended upon the elastic septal systeprotect dependent alveoli from compression, thereby reducing the usual gravitational gradient of lung expansio

Intra-pulmonary airways are devoid of cartilage, instead they appear to derive resistance to collapse from tetherinforces of the attached septa. 1997 Elsevier Science B.V.

Keywords: Elephant; L ung; Respiration; Anatomy; Histology; M echanics; Gravity; Pleural space

1. Introduction

While gravitational forces are known to influ-

ence the mechanics of respiration (see West and

M atthews, 1972; Bryan et al., 1966; M ilic-Emili et

al., 1966), we do not know if gravity has

influenced the design of the respiratory system

The elephant (El ephas maximus and L oxodonafricana), largest extant land animal and secononly to the largest whales in body mass, offers thopportunity to address important questions concerning the effects of gravity on the design of thmammalian respiratory system.

Unlike other mammals, elephants have beethought not to have an intrapleural space (Tod

* Corresponding author. Tel.: +1 617 667-3092; fax: +1

617 667-1500; e-mail: [email protected]

0034-5687/97/$17.00 1997 Elsevier Science B.V. All rights reserved.

PII S0034-5687(97)00038-8


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R.E. Brown et al./Respirati on Physiology 109 (1997) 177 194178

1913; Earles, 1929; Bugen, 1988). Descriptions of

attachments between lung and chest wall in ele-

phants (connections form in late fetal life, Earles,

1929) have been in the literature since 1682

(M oulin (1682) cited by Earles, 1929). Early spec-

ulations about the physiologic importance of

these connections (Todd, 1913; Earles, 1929),without apparent challenge in recent times (e.g.

see Short, 1962; von Beyer et al., 1990) revolve

around the elephants need for forceful inspira-tory efforts to inhale through the long nasal tubes

within the trunk and aspirate (and elevate) water

into their trunk for drinking. Both maneuvers

could require large transthoracic and trans-di-

aphragmatic pressures. It has been asserted that

such large trans-respiratory pressures could result

in a spontaneous pneumothorax or intrapleural

hemorrhage were it not for the connections be-tween the lung, chest wall and diaphragm (Todd,

1913; Earles, 1929; Short, 1962; von Beyer et al.,

1990). As wewill show, these assumptions are not

consistent with known respiratory mechanics.

Here we describe morphologic features (gross

to ultrastructural) of the elephants respiratory

system. We suggest that the morphology of the

elephants lung indicates that gravitational forcesdo indeed influence the design of the mammalian

respiratory system, at least in this large species.

The highly distensible connections between chestwall and lung cannot prevent a pneumothorax,

nor do they affect the movement of the lung

across thesurface of thechest wall during breath-

ing. Rather, the loose pleural space connective

tissue may be important in the regulation of the

flow of pleural fluid.

In the elephant the delicate gas exchanging

pulmonary parenchyma is compartmentalized

into grape-like units, 1 cm3, by an extensive

system of thick, elastic septa that originate from

the lungs external capsule and which ramifythroughout the lung. We suggest that the par-

enchymal compartments are suspended by the

elastic septa so that dependent areas of the lungs

are not compressed by the lung above, and non-

dependent alveoli are protected from overexpan-

sion, thus reducing theeffects of gravity acting on

the elephants tall lung.

2. Materials and methods

2.1. The animal

An 18 year old, 2140 kg, adult male Africa

elephant (L oxodonta africana) suffering fro

chronic, localized osteomyelitis, was euthanizewith alfentanyl, xylazine and phenobarbita

Other than the osteomyelitis no pathologic findings were encountered during the necropsy begu

immediately after death.

2.2. Thoracic dissection and gross obserations

With the animal in right lateral recumbenc

the left fore and hind limbs were removed an

the abdomen opened and eviscerated witho

penetrating the thoracic cavity. The thorax winitially opened and inspected via an incisio

through the left, dorso-lateral aspect of the d

aphragms central tendon and later through

2020 cm opening made by cutting section

from three ribs in the left caudal, dorso-later

rib cage (F ig. 1B). Following this, the left che

wall with its attached segment of diaphragm wa

removed from first to last rib, sternum to th

dorsal costal arch. Assessment of the mobilit

and deformability of the pleural connective ti

sue were completed at this time. Representativspecimens of central tendon, diaphragm muscl

intercostal muscle and costal periosteum we

harvested with attached pleural connective tissu

L ungs were removed en bloc with attache

trachea and heart. L ung tissue was sample

from all regions, deep to superficial, of bot

lungs. A primary bronchus and one of i

branches was serially sampled from where it en

tered the lungs hilum until it reached a diamet

of1.0 cm. A section of mid-trachea (intratho

racic) with five complete rings was preserved glutaraldehyde.

2.3. Tissue preparation

2.3.1. Fixation

Tissue specimens wererinsed with 0.05 M phophate buffer (pH 7.2) and fixed for 24 h wit


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R.E. Brown et al./Respirati on Physiology 109 (1997) 177 194 1

glutaraldehyde (3.0%, E.M . Grade, Tousimis) in

0.05 M phosphate buffer (pH 7.2) at ambient

temperature. The fixative was replaced twice

within the initial 4 h. Some tissue blocks were

stored in glutaraldehyde for later sub-gross dissec-

tion. Tissues for electron microscopy were post-

fixed in 1% osmium tetroxide in 0.05 Mcacodylate buffer (pH 7.2). All tissues for micro-

scopic examination were dehydrated in a graded

ethanolic series (70% to absolute).

Theelephants lung tissues were compared with

those of three domestic species: mature cattle and

horse, both 400 kg, and pig, 55 kg. Tissue

from healthy lungs was harvested at necropsy and

immersed in 10% buffered neutral formalin.

2.3.2. L ight microscopy

Specimens were processed according to stadard paraffin techniques. Sections, 6 m thicstained with hematoxylin and eosin, Verhoeff-VaGiesons and M assons Trichrome were photographed with a Nikon photomicroscop

M ontage reconstructions were accomplished usinoverlapping fields digitally photographed (10with a Dage 725 CCD camera on a L eitz photomicroscope into a Zeiss IBAS image analysis sytem. Individual fields were reassembled usinAdobe-Photoshop running on an Apple M acintosh, Quadra 605.

2.3.3. Transmission electron microscopy

Specimens were embedded in Spurrs resin acording to standard procedures. Thin section100 nm, stained with uranyl acetate and leacitrate were examined with a Phillips 300 electromicroscope.

3. Results

3.1. Gross obserations

3.1.1. The animal

The maximum external dimensions of the thorax (with the animal in lateral recumbency prio

to death) were: 118 cm transverse and 178 cventro-dorsal. The trunk, from its distal tip tapproximately the level of the palate, was 200 clong. Thenasal tubes within the trunk were highresistant to collapse; an investigator (101 kg) suported by one knee (68 cm2 of contact) on thdistal end of the trunk did not collapse the enclosed nasal tubes upon the researchers fingeinserted into the external nares.

3.1.2. Thoracic cai ty

A small (15 cm) initial incision through thdiaphragms central tendon immediately resultein a large pneumothorax (Fig. 1). Surrounding thpneumothorax cavity was a lustrous, smooth suface formed of pale-yellowish connective tissuThis grossly homogeneous, loose connective tissuwe refer to as pleural space connective tissu(PSCT). Through the chest-wall window in th

Fig. 1. Diagram of a section through the thorax of an African

elephant (L axodonta africana) in right lateral recumbency. (A )

Prior to opening the chest the lung is apposed to the chest wall

and diaphragm. Pleural space connective tissue in the closedchest would form a layer a few cm thick filling the pleural

space. (B) Thorax was initially opened and inspected through

a diaphragmatic incision, internal to which an open, tissuefree

space, i.e. pneumothorax, was observed. Prior to any further

disturbance to the thorax a 2020 cm window was made in

the lateral rib cage. T he large pneumothorax was surrounded

by a smooth surface of aerated pleural space connective tissue

that prevented us from seeing the surfaces or shape of the

lung, diaphragm or chest wall.


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caudo-dorsal rib cage (F ig. 1B), the PSCT sur-rounded a spherical pneumothorax cavity morethan twice thediameter of thechest wall window,beyond which no thoracic viscera were visable.Theaerated PSCT covered and filled all the spacebetween chest wall, fully collapsed lungs, di-

aphragm and pericardium. Note that the PSCTwould have had a much smaller volume in theintact (closed) chest before it became aerated bythe pneumothorax and resulting lung collapse(compare Fig. 1A and 1B).

When not stretched to its elastic limit, thePSCT was soft and could be easily deformed.However, when stretched as it was surroundingthe pneumothorax cavity it was extremely toughand could not bepenetrated by a finger. Handlingand dissecting the unstressed PSCT was difficult,due to its slickness and the ease with which itssubstance was sheared when attempting to pene-trate it. Examination of the lustrous PSCT at-tached to excised lungs and chest wall revealed itto contain myriad small spaces (fluid and airfilled) among the wet, shiny fibers; the gross ap-pearance was somewhat similar to a pad of wet,tightly woven, multi-layered surgical gauze. ThePSCT appeared grossly to be structurallyisotropic when aerated (two dimensionallyisotropic in the tangent plane when not aerated)and without any obvious macro structure.

3.1.3. Diaphragm

The diaphragms insertion extended from theventral end of the first pair of ribs caudo-dorsallyto the most dorsal aspect of the21st (last) rib. Themuscular portion of the diaphragm at mid-lateralthorax was approximately 3 cm thick and 17 cmlong from rib cage to central tendon.

3.1.4. Deformability and mobility of pleural space

connectie tissue

We assessed the degree to which the PSCTmight limit the mobility of the structures to whichit was attached by the following:1. Although the slimy PSCT was attached to and

appeared continuous between therib cage andthethoracic surfaceof thediaphragm muscle itdid not impede the diaphragm from beingelevated perpendicular to the inner surface of

Fig. 2. Diagram of a 2525 cm slab of the elephant d

aphragms central tendon lying on a surfacewith the attach

pleural space connective tissue uppermost. The surperfic

tissuelayer, grasped at oneedge of theslab, could bedisplac

(shear deformation) more than 17 cm without apparent

distrubing the next deeper layer.

the rib cage. With the diaphragm held perpen

dicular to the rib cage, the attached PSCT wa

not taut, but remained loose and easily d

formed.

2. A 33 cm section of the central edge of th

diaphragm muscle was isolated from su

rounding muscle, but not from the underlyin

PSCT loosely binding it to the inner rib cag

This piece of muscle could be slid easily bac

and forth, away from and towards the d

aphragms insertion on the rib cage, over

distance of 26 cm.3. A slab of the diaphragms central tendo

2525 cm, was isolated without displacin

the attached PSCT and placed with its abdom

inal side down (Fig. 2). At the midpoint alon

one edge of theslab, themost superficial (clo

est to lung in vivo) portion of the PSCT wa

grasped with forceps. The point of the forcep

grasping the PSCT could be easily moved to

wards the opposite side of the slab, creating

deep V shaped pattern in the superfici

PSCT, for a distance of 17 cm withodislocating or disturbing the immediate

deeper layers of PSCT. The PSCT, althoug

easily distended or deformed, was not elasti

for example, when the superficial layer wa

released it remained in its distorted V

configuration, retracting towards its origin

position by less than 2 cm.


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Fig. 3. Elephant lung, superficial relationships of macroscopic connective tissue components, light microscopy reconstruction, lun

fixed at zero stress. The lungs highly distensible external capsule (Ext C) is folded or pleated when under no tension. The pleur

space connective tissue (PSCT ) is attached evenly across the lungs external capsule. The distensible intralung septa (IL S) origina

from the lungs external capsule and ramify throughout the pulmonary parenchyma, dividing the parenchyma into compartmen

1 cm3.

After removing the lungs from the thorax,PSCT attached to the lung could be easilystretched to considerable lengths. A handful ofPSCT lying next to the lung in the unstressedstate could beeasily stretched uniaxially to 2050cm without disturbing (elevating) the surface ofthe lung itself. The elongated stem of PSCTraised from the lung surface, when released, didnot reform itself into the smooth layer coveringthe lung, but instead remained in a deformed,

elongated blob lying on the surface. The PSCTwas a very slimy material that stuck to mostthings it touched (e.g. latex gloves, table tops) butwas difficult to grasp because it was so easilysheared (deformed). A layer with an unstressed(but aerated) thickness of5 cm could be easilysqueezed between thumb and finger to a layer 1mm thick.

3.1.5. L ungs

The left and right lungs having one lobe each

were encapsulated with a thick and highly elasticlayer of dense connective tissue (F igs. 3, 4 and6A). The PSCT completely covered and was at-tached to this capsule, which is homologous withthe visceral pleura (albeit without a serosa, seebelow) covering the lungs of other animals. Iso-lated strips of the lungs thick, elastic capsulecould bestretched greater than twicetheir original

length and when released returned to their orignal highly folded configuration (Fig. 3). From thexternal capsule strong, elastic connective tissusepta ramified throughout the pulmonary paenchyma. All grossly visible intrapulmonary aiways were invested with a thick coat of denconnective tissue. The airways with their perbronchial connective tissuegavethecut surface othe lung a very rough, pebbly feel and appeareas if the walls of all airways contained abundan

cartilage, although no cartilage was found osubsequent microscopic examination. When thcut ends of small, 2.0 mm luminal diametairways were grasped with forceps considerabforce was needed to collapse the lumen. (This higresistance to thecollapse of small airways is notfeature of the lungs of pig, cow, horse, human omost other terrestrial animals.)

3.1.6. Trachea

The lumen of the mid-trachea, 7.55.5 cm

was supported by massivecartilaginousrings (Fi5). The end of each incomplete ring articulatewith its other end and the opposite end of one othe adjacent rings. This produced a helical arangement of the tracheal rings, the overlappealternating attachments making a saw-tooth patern (zipper like) along the tracheas dorsal suface. The dorsal third (both sides) of each rin


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Fig. 4. Elephant lung 15 cm deep from its pleural surface showing macroscopic relationships of connective tissue componen

light microscopy reconstruction, fixed under zero stress. Thedistensible intralungsepta(IL S) ramify extensively throughout thelun

dividing the pulmonary parenchyma into compartments 1 cm3. The intralung septa when under no tension, as in th

reconstruction, are folded and pleated. Note that the vessels (V) and bronchi (B) with luminal diameters 0.1 mm are attach

within and surrounded by the supporting framework of the intralung septa. When this figure and F ig. 3 are compared, it may

noted that the intralung septa occur in a range of thicknesses from that exceeding that of the lungs external capsule down to th

only somewhat thicker than an alveolar septum.

overlapped substantially with the two adjacent

rings. Thus, the borders of the rings were not

parallel. The rings cross-sectional shape (in

planes passing through the airway axis) variedfrom a thick oval with a convex external surface

ventrally to that of a flattened oval cross section

laterally, ending with irregular facets for their

double articulation dorsally. The rings were fixed

to one another in the overlapping areas and

across their articulations by tough fibrous tissue.

The tracheal mucosa had many 1 mm deep

longitudinal rugae. These rugaecould conceivably

result from constriction of the trachea by contrac-

tion of the very thin (relative to that of 500 kg

cattle) band of trachealis muscle, 1.5 cm long,which was inserted on the unyielding luminal

surface of the rings, spanning their articulated

ends. However, the fibrous tissue fixing the rings

dorsally and the thinness of the trachealis muscle

make this seem unlikely, and we believe that the

tracheal conformation wesaw postmortemexisted

in vivo. The cartilaginous rings supporting the

trachea and extrapulmonary primary bronc

ended at the lung hilum.

3.2.Subgross dissection of lung ti ssue blocks

Blocks of lung, 211 cm, fixed in glu

taraldehyde were dissected and microscopical

examined at 10 40. The fixed PSCT, thoug

less distensible than when fresh, could be easi

deformed and elongated to more than twice i

fixed-resting length. The PSCT appeared as

complex, 3-D fibrous network containing myria

air- and fluid-filled spaces 0.1 mm3; the spac

between fibers occupied a larger volume than th

formed elements.In most areas thecollapsed lungs external cap

sule was finely folded or pleated (Fig. 3). Th

connective tissue septa seen on gross dissectio

partitioned the pulmonary parenchyma into iso

lated compartments of about 1.0 cm3 (Figs. 3,

and 6D). We term these septa intralung septa t

distinguish them from the alveolar septa compri


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ing the parenchyma. The fixed parenchyma couldbe easily scraped from the septa leaving strong-walled cavities. Commonly the thicker intralungsepta could be easily separated into two distinct,tough layers between which were found scattered,loose collagenous attachments. Airways and ves-

sels within the lung were invested with denseconnective tissue continuous with the septa (Figs.3, 4 and 8A). Each parenchymal compartmentwas apparently supplied by a single airway andvascular branch. These compartmental branchesdiverged from their parental airway or vessel (lo-cated within an adjacent intralung septum) and

coursed to the center of the parenchymal com

partment before giving off a cluster of termin

branches. These compartmental branches an

their terminal ramifications (to thelimit of micro

scopic observation) were covered by a reflectio

of intralung septal tissue (Fig. 8A).

3.3. M icroscopic anatomy

3.3.1. PSCT

Other than the surface of the pericardium

contact with the heart, no mesothelial (serosa

lining was found within the thoracic specimen

including samples of the lungs external capsu

deep to the PSCT, the PSCT and the intern

chest wall and diaphragm (Fig. 6A and 6C). How

ever, we found a normal appearing serosa inves

ing the abdominal surface of the diaphragm.The PSCT, including its attachments to th

external lung capsule, diaphragm and internal su

faces of chest wall, was almost entirely collag

nous with but an occasional elastin fiber (1 p

40 field) found within its structure where

joined the intercostal membrane. The intercost

membrane was a bi-layered structure, each lay

of which appeared similar in thickness and elast

content to the lungs external capsule. Whereas

most of the PSCT there was no apparent organ

zation of thecollagen fibers of thePSCT (Fig. 6and 6C), in some areas small bundles of collage

fibers were found to join and diverge in a chicke

wire like arrangement (Fig. 6B).

An abundance of small vessels, capillaries an

perhaps lymphatic ducts, were found througho

the PSCT (Fig. 6B and 6C). The number of the

vessels appeared excessive for the almost neglig

ble metabolic needs of this collagenous tissu

Dispite the much greater density of formed el

ments in the lung capsule relative to the pleur

space, there were about 7-times as many vesseper field in the loose PSCT, 7.5 per field, as

thelung capsule. Further, about 1/2 of thevesse

found within the lung capsule itself were foun

within the 15% of the capsule nearest the PSCT

Examination of the dense, pure collagenous ti

sues of the diaphragms central tendon and cost

periosteum showed 0.3 vessel per field.

Fig. 5. Segement of elephant trachea taken midway from

larynx to carina. (A) Perspective of complete trachea, dorsal

aspect foremost. (B) M id-sagital section of ventral aspect. (C)

Cross section with dorsal aspect at bottom. The cartilaginous

rings supporting the lumen are overlapped by 25+% of their

width along the tracheas lateral aspect (see cut off rings,

cross-hatched in (A). The overlap is reinforced with a dense

fibrous aponeurosis (FA) connecting adjacent rings. Over the

ventral aspect of thetrachea therings do not overlap (see Fig.

B) but continue to bestrongly united by the fibrous aponeuro-

sis. With a saw- tooth-like appearance, the end of each carti-laginous ring articulates with (1) its opposite end, (2) the

opposite end of the adjacent ring and (3) continues to be

overlapped with its adjacent member. The interlocked ends of

the cartilaginous rings, similar to an osseous articulation, are

supported by tough fibrous tissue (FA in C). Note that the

cross-sectional shape of the cartilagenous rings changes con-

siderably as one moves around their circumference. The tra-

cheal mucosa (M) is strongly pleated into numerous

longitudinal rugae.


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Fig. 6. Elephant lung, light microscopy, Verhoeff-Van Giesons elastin stain, collagen red, elastin black, smooth muscle brown. (A

Filling the center of the figure is the dense and highly distensible external capsule of the elephants lung. The external capsule h

an elastin (black) content of at least 35% relative to that of collagen (red). Across thetop of thefigure, external to thelungs extern

capsule, is the diffuse, unorganized pleural space connective tissue (ct) composed entirely of collagen. Note the absence of a

serosal surface on the external surface of the elephants lung or within the pleural space connective tissue. The pulmona

parenchyma along thefigures lower edge is divided by oneintralung septum originating from thelungs external capsule. Compa

the thickness of the elephant lungs external capsule in this figure with that of the large domestic animals visible in Fig. 8D. (

Thepleural space connective tissue, in some areas appeared to have some microscopic organization (see text for details). M any sma

vessels (identified by their endothelial cells) can be found throughout the pleural space connective tissue. (C) The collagenous b

highly distensible pleural space connective tissue is less organized in this view than in B, contained far more capillaries a

lymphatics that required for the metabolic demands of this fibrous tissue. The lungs external capsule crosses the lower, left corn

of this figure. (D) Thebranching (three) point of an intralung septum surrounded by distorted and collapsed parenchyma. Notethigh elastin (black) content of the distensible intralung septum.

3.3.2. Capsule and septal system of lung

The lung was enclosed within a thick (mean0.70 mm, range 0.25 1.75 mm) capsule com-posed of 35 50% elastin and 50 65% collagen(surface area approximations) (Figs. 3 and 6AFig.

7). Intralung septa, with a fibrous arrangemensimilar to that of the lungs external capsule, wecontinuous with the fibrous components of thexternal capsule (Figs. 3, 4 and 6A and 6D). T hthickness of intralung septa varied from tho


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equal to thelungs external capule to those only afew times thicker than an alveolar membrane. Thethickness of a septum appeared to beindependentof its position; thick and thin septa could befound both at the lung surface attached to theexternal capsule and deep within the lung. The

elephant was found to have24 times the numberof intralung septal surfaces per field as did thedomestic animals examined for this study, al-though it is important to remember that there wasan unknown degree of lung collapse in all theexamined animals.

All pulmonary vessels larger than capillariesand all non-respiratory airways were enclosedwithin intralung septa (Figs. 3, 4 and 8AFig. 9).The fibrous tissue of a septum was continuouswith the fibrous tissue forming the wall of thevessel or airway. The fibrous tissue layer sur-rounding airways and vessels contained copiousamounts of elastin external to themuscularis (Fig.8A). L arger vessels and airways were often lo-cated within the junction of two or more septa.

3.3.3. A irways

Except for the initial 5 cm of the intrapul-monary primary bronchus around which isolatedcartilaginous plates could be identified, the intra-

pulmonary airways were devoid of cartilaginoutissue. The latter was surprising considering thpebbly feel of the lungs cut surface and the fathat cartilage is a prominent intrapulmonary aiway component in other species, including thhorse, cow and pig.

A circumferential sheath of dense connectivtissue, continuous with and identical in appeaanceto the intralung septa, surrounded the largairways (2 mm luminal dia) (F ig. 9). A layer oadiposetissue crossed by many radial collagenoubands (peribronchial tissue in Fig. 9) separatethe airways septal sheath from its thick waSepta radiated from the sheath in the plane of thairways axis and continued into the pulmonarparenchyma.

Smaller airways (2 mm luminal dia) wealways tightly invested within a septum (Figs. 3, and 8A). The fibrous tissues of the airway anassociated septum combined to create thick aiway walls whose thickness external to themucoswas 30 200% that of the luminal diameter. Bcontrast, terminal bronchioles leading to alveoladucts had wall thicknesses a small fraction of thluminal diameter, similar to the airways from thother taxa examined for this study (F ig. 8B).

The mucosa of all airways larger than terminbronchioles was folded creating long, narrow, axially orientated crypts (Fig. 8A,Fig. 9) that mim

the mucosal rosetts found in lungs that are in aactively broncho-constricted state. We estimathat the surface created by the pleated mucoswas sufficient to smoothly cover a tube 2times the observed diameter of that airway. Thmucosa contained an abundance of goblet cel(Fig. 8A). A film of amorphous material, assumeto be mucus, coated the mucosa in most airwayand rarely polymorphonuclear cell were foun(1 per 40 field). The submucosal and musclaris layers of the airway walls contained an abun

dance of elastin fibers relative to that of the othtaxa examined (Fig. 8A and 8BF ig. 9). T heorientation of the submucosal elastin fibers was prdominantly axial (mostly cross-sections of fibewere found in airway cross-sections), with thelastin fibers of the submuscularis and attacheintralung septa oriented morenearly radially (logitudinal sections of fibers found in cross-section

Fig. 7. Elephant intralung septa, transmission electron mi-

crograph. The highly distensible intralung septa are composed

of35% (50% in this view) amorphous elastin fibers (E)

with the remainder being bundles of collagen fibers (C) and

the occasional fibroblast (upper left). Bar=1 m.


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Fig. 8. Elephant lung, light microscopy, Verhoeff-Van Giesons elastin stain. (A) Smaller conducting bronchuswith attached septumThe mucosa of the airways in these lungs fixed at zero stress was always found highly pleated. The majority of the submucos

elastin fibers (black) have an axial orientation, in contrast to the elastin fibers of the attached intralung septum which are radial

the airway. sm, airway smooth muscle. (B) Terminal bronchiole and alveolar duct. Numerous, axially oriented elastin fibers lyin

deep to the airways mucosa (arrowhead) continue into the alveolar duct (top 3/4 of figure). T he pulmonary parenchyma is high

distorted and collapsed in these lungs fixed at zero stress (relaxed). N ote the magnification of this figure is twice that of all oth

color micrographs. (C) These three micrographs represent one complete and continuous slice through the diaphragms centr

tendon from abdominal (1) to thoracic (4) sides (about 10% of the central tendons thickness is not represented in these thr

micrographs). The central tendon, 3.0 mm thick, was composed of three distinct and separate layers only loosely joined b

occasional collagen fibers (see left side of 3-4). The layer on the abdominal side of the central tendon (1-2), invested with a seros

membrane(not shown), was theonly layer to contain elastin fibers. Pleural spaceconnectivetissuewas attached to 4 side of sectio

3-4. (D) External lung capsule of cow (D1), pig (D2) and horse (D3). Compare these with the elephants much thicker and dens

external lung capsule seen in F ig. 6A. In addition, the elephants external capsule contained much more elastin. All micrographs

external lung capsule, e.g. F ig. 6A and D of this figure were stained simultaneously and are shown at identical final magnificatio

of airways). The submucosa of terminal bronchi

contained abundant, axially-oriented elastin

fibers that continued into the alveolar ducts(Fig. 8B).

3.3.4. Gas exchange tissues

The lungs were collapsed at the time of initi

examination and during fixation; thus the fin

alveolar architecture was distorted or obscure


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Fig. 9. Intralung septa tethering a large airway. All airwayshad one or moreintralung septa (IL S) attached to, and radiatingnorm

to the airways axis. In the larger airways, such as the one shown here, the multiple septa were attached to the airway via

circumferential septum that enclosed a zone of interwoven collagenous fibers and adipose tissue (peribronchial tissue). T

submucosal layer contained large numbers of predominantly axially oriented elastin fibers, seen here as a thick dense-black ba

deep to the airways pleated mucosa (M ).

(Fig. 6DF ig. 8BFig. 10). M any collagen fibers and

bundles of collagen fibers were found immediately

beneath the pulmonary epithelium and deeperwithin the alveolar membranes (Fig. 10). The

apparently increased collagen content notwith-

standing, the elephants alveolar membranes, type

1 and 2 pulmonary epithelial cells and capillaries,

appeared like those of other mammals. Gas ex-

change tissue lined the intralung septa.

3.3.5. I nflammator y cell s

Alveolar macrophages were found within the

elephants lung. M ononuclear cells found within

alveolar capillaries have provisionally been iden-tified as pulmonary intravascular macrophages

(Fig. 10).

3.3.6. Diaphragm

The central tendon over 3 mm thick was com-

posed of three distinct layers of dense, collage-

nous tissue. The layer nearest the abdomen also

contained some elastin fibers mingled among thcollagen fibers (Fig. 8C). Electron microscopy r

vealed a highly anisotropic arrangement of thcollagen fibers within each of the layers, and ligmicrographs suggested a different orientation othe fibers in the different layers. The three layewere loosely joined by diffuse collagen fibers.

3.4. Comparatie morphology

In conjunction with the present study the lungof domestic cow, horse, and pig were examinehistologically (Fig. 8D). In these domestic anmals, the lungs external fibrous capsule was a

ways less than 0.18 mm thick (elephants capsuwas 0.25 1.75mm thick) and only rarely weelastin fibers identified (elephants capsule waelastin rich). The intralung septa of these animawere commonly composed of two thin collagnous sheets, which together were always less tha0.08 mm thick (not counting any gap betweelayers), and only very rarely contained elast


12/18


fibers. In contrast, the elephants elastin rich in-tralung septa were found in a range of thicknessesup to that of its external lung capsule. The inter-lung septa of the domestic taxa were only infre-quently found to attach to an airway. In sharpcontrast to those of the elephant, the larger intra-

pulmonary airways of these domestic animalscontained cartilaginous rings while smaller, non-respiratory airways contained cartilaginous plates.The thickness of the walls of smaller airways inthese domestic animals was25% of theairwayssubmucosal diameter (elephants airway wallswere 30 200% of submucosal diameter). Relativeto those of theelephant, the wall of theairwaysofthese domestic animals contained very few elastinfibers.

3.5. Critique of methods

Although we thoroughly examined the thoraciccompartment and many areas within thelung, thisstudy presents data on a single animal. In addi-tion, except for examining the mobility of thePSCT , we have no in vivo or in situ experimentalmeasurements of the mechanics of the elephants

respiratory system. The histologic findings rsulted from a random sampling of the lung sthat a comprehensive morphometric evaluation othe regional differences in lung morphology wanot possible.

4. Discussion

4.1. M echanics of breathi ng and t he elephants

pleural space connectie tissue

4.1.1. L ung moement relatie to chest wall

duri ng breathing

The mobility, extreme compliance, ease oshearing and slipperiness of the pleural space connective tissue(PSCT ) implies that it has negligibinfluence on the sliding motions of the lung relative to the chest wall during breathing. Thus, thlung is free to slide relative to the chest wadiaphragm, mediastinum, and movein and out othe costophrenic sulcus. Also the fact that thlungs immediately collapse producing a largpneumothorax via a small incision through thdiaphragm with an otherwise intact chest wademonstrates, that the highly deformable PSCdoes not restrict lung movement and cannomaintain the lungs in their inflated configuratioin the absence of an intact lung and chest wall, i.

the pleural space must be closed for the elephanto breath.

In that the elephants chest lacks both viscerand parietal mesothelial (serosal) surfaces, and ilung, albeit loosely, is attached to the chest waone could argue that the elephant lacks a pleurspace. On the contrary, the elephant does possea functional pleural space that allows independenmovement between lung, chest wall and daphragm, functioning identically to the liquidlined pleural space of other mammals. Unique t

the elephants pleural space is that it is finedivided by the fibrous continuum of PSCT, thfibers of which are lubricated by the elephantpleural fluid.

We consider thedeformability or stretchiness othe PSCT to bea function of thenetwork organzation of its fibers which are almost entirely inelastic collagen. While the ease with which it ca

Fig. 10. Elephants alveolar septum, transmission electron

micrograph. Note the large quantity of collagen fibers and

bundles of collagen fibers (arrowheads) lying between the

pulmonary epithelium (PE ) and capillary endothelium (CE).

We have provisionally identified the large mononuclear cell

filling the capillary lumen as a pulmonary intravascular

macrophage. Bar=1 m.


13/18


be sheared is, quite frankly, amazing, there areother examples (different taxa and differentanatomical locations) in which networks of colla-gen fibers undergo large physiologic deforma-tions. A common example is the subcutaneoustissue attaching skin to underlying muscle fascia,

e.g. the domestic cats thigh and knee can movecranio-caudally 15 cm beneath the skin of theflank without disturbing the overlying skin.

4.1.2. Eleating water ia the trunk during

drinking

Speculations in the literature suggest that theconnections between theelephants lung and chestwall, i.e. PSCT are necessary to prevent a sponta-neous pneumothorax and pleural vessel hemor-rhage from occurring secondary to eitherelevating water in the trunk for drinking or force-ful inhalations against a high resistance to flowthrough the long trunk (we consider a high resis-tance to airflow doubtful but no measurementsare available) (Todd, 1913; Earles, 1929; Short,1962; von Beyer et al., 1990). L arge trans-respira-tory pressure differences (from alveolar space tobody surface), up to 300 cmH20 in a large ele-phant completely filling its nasal tubes to the levelof thepalate, would beborn by the chest wall anddiaphragm as the elephant aspirated water up thetrunk with its respiratory muscles. We assume (1)

that elephants nearly fill their trunks with waterand (2) that they use ventilatory muscles ratherthan lingual and facial muscles. Y et, the pressuredifference between alveolar space and pleuralspace (transpulmonary) tending to distend pul-monary parenchyma is strictly a function of lungvolume and is governed entirely by the elasticrecoil properties of the lung per se. It follows thatthe elephants transpulmonary pressures are unaf-fected by drinking and thus the likelihood of aspontaneous pneumothorax (breech of pleural in-

tegrity) is not only no higher than that of otheranimals but probably much lower because of theelephant lungs very thick external capsule. Fur-ther, cavitation (i.e. separation of tissues due toextremely low pressure) within the elephantspleural space secondary to large transthoracicpressuredifferences cannot occur at absolute pres-sures above 50 torr (710 torr relative to atmo-

sphere); such pressures are remote from thoanticipated during drinking in even the largeelephants. Thus, with a closed pleural space thelephants lungs do not need, nor do they hav(see above) any attachments to the chest wacapable of preventing a pneumothorax while el

vating water in the trunk or overcoming higresistances to inspiratory airflow.

4.2. M echanical impli cations of eleating water i

a long trunk

However the extraordinarily low intrapumonary air pressures, 300 cmH2O, required televate water to a height of 3 m in the nasal tubwith respiratory muscles could potentially (1) colapse the extrathoracic trachea or nasal tubes, (2injure the diaphragm (muscle, central tendon) ochest wall or (3) cause blood shifts or othcardiovascular effects (not discussed).

4.2.1. Nasal tubes and trachea

Water aspiration to heights up to 3 m is possble only if the extra-thoracic trachea and nastubes within the flexible trunk can resist collapfrom such large transmural pressure differenceThe resistance to collapse of the muscular anconnective tissue elements forming the trunwhich has no ossified tissue are a function of th

trunks thickness. An indication that the trunk sufficiently resistant to collapse is that a loccompressive stress 6.0103 cmH2O failed tcollapse the distal nasal tubes where the trunkwall is thinnest. Collapse of the extra-thoractrachea is prevented by the massive tracheal ringwhich are functionally completeby virture of theinterlocked ends in addition to the overlap btween adjacent rings. The intrathoracic trachelike the lung, is not affected by the trans-respirtory pressures associated with elevating water

the trunk for drinking.

4.2.2. Diaphragm and chest wall

Production and support of thetrans-respiratorpressure differences necessary to elevate water tthe top of the trunk is no mean feat and suggesthe presence of special structural modificationwithin the elephants chest wall, i.e. ribs, inte


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costal muscles and diaphragm. While we have no

information concerning the mechanical properties

of the ribs and intercostal muscles (gross and

histological examination of theintercostal muscles

were unremarkable), there are several features of

the elephants diaphragm that may assist in the

production and support of those forces. Thethick, well developed, trilaminar structure of the

elephant diaphragms central tendon appears to

bean adaptation for the support of large trans-di-

aphragmatic pressures (Fig. 8C). Sacks and

Chuong (1992) describe the organization of the

collagen fibers of the single layered central tendon

of other mammals as orthotropic (having parallel

fibers; see also Griffiths et al., 1992). There is a

weakness with such an arrangement in that a

rupture or separation could occur between fibers

at forces far below those required to break thefibers themselves. Whereas the collagen fibers of

each individual layer of the elephants central

tendon are also in a parallel arrangement, the

different alignments of the fibers in the three

layers of theelephants central tendon would con-

fer nearly isotropic mechanical properties to this

trilaminate structure.

The elephants diaphragmatic muscle appears

to be well adapted for the generation of large

forces and thus pressures. Using approximations

of the internal dimensions of the elephants chest

(taken here to be lateral=100 cm and ventrodor-

sal=143 cm) wecan calculatetheoval circumfer-

ence (388 cm) and axially projected area of the

diaphragm (Areadi) to be 1.12104 cm2. From

the internal circumference of the chest wall and

thickness of thediaphragmatic muscle (taken here

to be 3 cm) we can calculate the total cross

sectional area of the muscle (CSAM) to be 1.16

103 cm2. (This underestimates both projected area

and muscle cross-sectional area because of theoblique orientation of the elephants diaphragm.)

Assuming the elephants diaphragmatic muscle

generates a maximal stress () (tension) similar to

other animals skeletal muscles (2106 dynes/

cm2; Powell et al., 1984), wecalculatethemaximal

pressure (Pdi) that this elephants diaphragm can

produce is

Pdi=M CSAM

Areadi 200 cmH2O

The orientation of the surface of the elephantdiaphragm is oblique (nearly 45) to the spinaxis (and gravitation force), in contrast to thmore perpendicularly disposed diaphragms o

other animals. This may represent an adaptatiofor the appropriate generation of pressures involved in drinking, or an adaptation for the suport of the static pressure gradients associatewith gravity acting on the very different densitiof thoracic and abdominal viscera. These possibiities remain uncertain and deserve further study

4.3. The elephants respiratory system:

adaptations to grait ational str ess

Thequestion, Do gravitational forces set limion the design of the respiratory system? (L eith1976), has been long standing in respiratory phyiology. At least two features of the elephantrespiratory system appear to bestructural adapttions for the amelioration of the effects of gravit(1) capsule and intralung septal system and (PSCT.

4.3.1. Capsule and i ntr alung septal system of lun

The total pressure difference (P) from the to

to the bottom of the lung resulting from graviand tending to collapse dependent alveoli anhyperexpand superior parenchymal tissue increases directly with the height of the lung: P=pgh, where p, tissue density, g, acceleration due tgravity and h, height of lung. West and M atthew(1972) described that in most mammals there isregional (top to bottom) difference in alveolainflation existing at low lung volumes resultinfrom the compressive effects of gravity, but thas lung volume is increased the regional diffe

ences would disappear due to a stiffening effecdue to the parenchymas nonlinear stress-stracharacteristic (see Radford, 1957). That is, as thalveoli in thesuperior areas of thelung reach themaximum volume their stiffened parenchymcomponents forcefurther inflation to occur in thmore dependent and less distended regions of thlung.


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In theelephant, thepressures inflating thealve-oli would vary by 50 cmH2O from the top to thebottom of the lung estimated to be 145 cm tall atits maximum (in vivo density of lung taken to be=0.35gm/cm3; see G anesan et al., 1995). As-suming the elephants lung has a pressure-volume

relationship similar to that found in other mam-mals in which the vital capacity spans a transpul-monary pressure range of 2530 cmH2O, the 50cmH2O pressuredifference from top to bottom ofits tall lung would mean that there would be norange of lung volumes at which both uppermostand lowermost alveoli would experience physio-logically normal distending pressures duringbreathing. It follows that at all physiologic lungvolumes, the elephants tall lung, without struc-tural modifications, would have a large propor-tion of its dependent alveoli collapsed and a largeproportion of its superior alveoli over-distendedor highly stressed.

Here, it is important to distinguish between thevertical gradient in pleural pressure, Ppl, whichsupports the whole lung in gravity, and the verti-cal gradient in distending pressure of the pul-monary parenchyma, which we argue for theelephant must besubstantially less than Ppl. In thelungs of other (smaller) mammals it is argued thatthe pressure distending the parenchyma is theelastic recoil pressure of thelung,Pel

(L)

=PAPpl(M ead et al., 1970) where PA is alveolar pressure.This pressure is also the stress within the par-enchyma averaged over an area transecting manyalveoli (e.g. several mm2). In the elephant thisassumption may not hold; within the small par-enchymal units stresses averaged over several mm2

may be substantially less than the stresses withinthe lung and its supporting intra-lung septal sys-tem averaged over many cm2. At least in verylargelungs it appears unreasonable to expect lungtissue to be self supporting. If the mass of par-

enchyma, blood supply and airways comprisingthe elephants lung were to be supported solelyfrom fine internal structures at the alveolar andductal level it seems reasonable to expect consid-erable reinforcement within the lung. In fact, ele-ments capable of supporting compressive stresswould be necessary within its dependent portions.Such a structural adaptation at the level of the

alveolar membrane has not been found, or norecognized, in large mammals (including the elphant).

We suggest that theelephant lungs capsule anintralung septal system is a structural mechanisthat supports parenchymal, vascular and airwa

structures so that the alveoli are functionally isolated (partially or totally) from the gravitatioeffectsdescribed above. Thethick external capsu(visceral pleura) of theelephants lung, apposed tthe chest wall and diaphragm by virtue of a closepleural space as in other mamals, serves as foundation upon which to anchor the intralunsepta (Figs. 3, 4 and 6A and 6D). The extensivramification of theintralung septa throughout thpulmonary parenchyma serves as a space fillininterconnected set of surfaces tessellating the lunand supporting the resulting small (1 cm3) mchanically isolated compartments of parenchym

The high elastin content and coextensive nework of collagen and elastin fibers found in thelephant lungs intralung septa (and external casule) (Fig. 6A and 6DF ig. 7) is very similar to thafound in mammalian L ig. nuchae and the birdL ig. propatagiale. Those highly distensible, elastligaments have long, linear segments of theforce-length curves which enable physiologchanges in strain to beaccompanied by very smachanges in stress (Brown et al., 1994). In shar

contrast, pulmonary parenchymal strips havbeen shown to stiffen rapidly with very smaincreases in strain within their physiologic rang(Radford, 1957). The collagen and elastin composite forming the structural elements of the elphant lungs external capsule and intralung septsystem would allow these structures to maintanearly constant support of the pulmonary paenchyma across a wide range of lung volumeFurthermore, such pre-stress of the highly elasttissue of the septa need not substantially redu

the compliance of the lung during volume expansion. That is to say, if pre-stress of the septsystem at low lung volume were such as to supend parenchymal compartments uniformly, thewould be little regional difference in the inflatioof the elephants alveoli over a widerange of lunvolumes. Indication that prestress conditions dexist within the elephant lungs highly elastic ex


16/18


ternal capsule and intralung septa is reflected intheir tightly folded (pleated) conformation seen inthe deflated, relatively gas free lung and in iso-lated tissue blocks.

The linear elastic support mechanism providedover theentire lung by theelephant lungs capsule

and intralung septal system is quite different fromthe strongly nonlinear properties ascribed to theself- supporting parenchymal tissue of othermammals (see Radford, 1957; M ead, 1961; M eadet al., 1970; West and M atthews, 1972). We wouldexpect the compliance of the elephants pul-monary parenchyma within a single parenchymalcompartment to be similar to that of other mam-mals and its total lung compliance (governed bythe linear elastic force-length properties of septalsystem) to be similar to that of other mammals.That is, the elephants vital capacity could span arange of 25 30 cmH2O as found in other mam-mals. However, if the elephant is to experienceventilation of all its alveoli, its lung-wide meandistending pressure (as well as Ppl) must be higherthan other animals, at least 50 cmH2O.

Over a 7-fold range of body mass there ap-peared to be no difference in external capsule orintralung septal thickness among the domesticanimals. Additionally, the external capsule andintralung septa of the domestic animals was al-most entirely collagenous. Y et between cattle and

elephant (5-fold difference in body mass) therewas more than a 3-fold difference in capsulethickness and an order of magnitude difference inaverage septal thickness (compare Fig. 6A, D,Fig. 8D). Additionally, the elephants lung has24 times the density of intralung septa. Thoseresults indicate that above a certain size, lungparenchymal tissue itself may not be self-support-ing in the fashion described by M ilic-Emili et al.(1966) and West and M atthews (1972). This tran-sitional size appears to be one at which the differ-

ence in average recoil pressures between the topand bottom of the lung approaches the differencein recoil pressures between relatively un- inflatedand fully-inflated parenchyma. The very sparse(5%) elastin content of the intralung septa ofthe pig, cow and horse (and many other mam-mals, data not presented here), relative to that ofthe elephant (35 50%), indicates that the pul-

monary mechanics of those species is governed ba parenchymal force-length relationship similar tthat measured by Radford (1957); i.e. the nearinextensible alveolar septa dominate overall lunrecoil. In the domestic species the inelastic sepwould function in parallel with the inelastic alv

olar septa at high stresses.

4.3.2. Elastin content in walls of large airways

and essels

The walls and investing septa surrounding thelephants intrapulmonary airways and vessecontain many axially oriented elastin fibers (Fi8A). If the extensibility of the elephants intrapumonary airways and vessels is matched to that othe capsule and intralung septal system all thecomponents would contribute to the mechanicsupport of the pulmonary parenchyma. WhiHoppin et al. (1977) demonstrated that intrapumonary mechanisms exist to isolate and protethebronchial tree from axial distortion, we wousuggest that the elephants elastic bronchial treundergoes considerable length changes. L ai-F oo(1979) indicates that the larger arteries within thlung, function to limit regional expansion of pumonary parenchyma, contributing to the pumonary interdependence described by M ea(1961) and M ead et al. (1970). However, the denelastic coat of the elephants pulmonary vascula

tureand theseptal tissues investing it indicateththese vessels are quite extensible and that theprobably lengthen as the surrounding tissue expands, contributing to local pressure-volumcharacteristics without limiting expansion.

4.3.3. Fl ow of pleural fluid

Pleural fluid, under gravitational influences, exhibits at most a hydraulic gradient from the toof the lung to the more dependent areas of thintrapleural space(Lai-F ook et al., 1984; M isero

chi et al., 1988). Departures of liquid pressugradients from 1 cmH2O/cm vertical height havbeen associated with viscous pressure losses ariing from pleural fluid drainage (Lai-F ook anRodarte, 1991) and may also be involved witpumping of pleural fluid secondary to oscillatinshear stresses during breathing (Butler et a1995). We suggest that the fibrous matrix of th


17/18


PSCT (Fig. 6A, 6B and 6C) may be necessary toretard gravitationally driven flow of pleural fluidfrom top to bottom of the elephants tall lung,which could result in excessive thinning of thelubricating layer of liquid between lung and chestwall and collections of pleural fluid in the ventral

thorax.The myriad small spaces within the fibrouscontinuum of the PSCT may act to slow the flowof pleural fluid via a process of percolationthrough thefibrous matrix. Thus, the pleural fluidwould act as a lubricant between lung and chestwall by lubricating the motion between adjacentfibers of the PSCT. The abundance of small ves-sels and lymphatics (Fig. 6B and 6C) throughoutthePSCT suggest that large local fluxes of pleuralfluid occur within the tissues fibrous matrix.Thus, in contrast to the pattern of pleural fluidflow in other mammals with a fluid filled pleuralspace, the elephants pleural fluid may be pro-duced and reabsorbed locally, reducing or elimi-nating the flux of fluid from top to bottom of thethorax.

4.4. M aintenance of airway patency and the

elephants i ntralung septa

During expiration, when the pressure drivingflow is coupled to peribronchial pressure, flow

limitation could potentially occur in any unsup-ported intra-thoracic airway. In contrast to othermammals, the elephant has no cartilaginous sup-port of its intrapulmonary airways to maintainairway patency. However, theelephants intralungsepta which surround and attach to airwayslargerthan about 2 mm luminal dia. radiate normal tothe airways axis and ultimately connect to thelungs external capsule, suggesting that the lumi-nal patency of these larger airways may be main-tained by a tethering mechanism (Fig. 9). L uminal

patency of the smallest divisions of the bronchialtree, e.g. terminal bronchioles and alveolar ducts,in elephants (see below) as in other animals, isprobably maintained by local radial tetheringforces of the alveolar septa. However, the tether-ing open of the larger airways is by their attachedintralung septa and is not dependent on localparenchymal tissue. The highly elastic intralung

septa, with a nearly linear force-length relationship in their range of physiologic lengths, coupreserve airway patency at all lung volumes. Thmay represent an alternative adaptation for thairway luminal support provided by cartilage other mammals.

In the small respiratory and terminal broncholes airway patency must be maintained solely bthe local radial tethering forces of attached alvolar membranes in a fashion identical to that oother mammals (Fig. 8B). M any small bronch2 mm luminal dia., which in other mammawould be supported by cartilaginous plates, haonly one or two tethering intralung septa, so aalternative mechanism of luminal support may boperative in the smaller airways. The thick, bnon-cartilaginous, walls of these small airwayand their associated, investing septal tissues produce airways that are surprisingly resistant tcollapse and that produce a pebbly texture to thcut surface of the lung. Thebending stiffness of material is a direct function of its thickness, sthat the thick, dense walls of the smaller airwaymay protect their lumens from collapse. The relatively gas-free state of the intact lungs followintheir removal from the thorax was evidence thsmall airways remained patent at very low ditending pressures.

Interestingly, the folding pattern of the el

phants airway mucosa, apparently resulting froreductions in airway diameter with theunopposeelastic recoil of the septal and capsular tissu(Fig. 8AFig. 9), appear identical to the mucosrosetts that occur coincident with the bronchoconstriction produced by activation of airwasmooth muscle. With reductions in airway calibto the degree responsible for the observed mucosal folding, there would be substantial increasin airway wall thickness. It is possible that thelephants airway walls in vivo were no thicke

than comparable airways in other animals. If this the case it may be that the resistance to compression of the elephants smaller airways, as weas its larger airways, is conferred by the raditraction of the attached intralung septa.

We suggest that the development of the highelastic and extensive capsule and septa system othe elephant lung was driven by gravitation


18/18


demands for parenchymal support, but that withattachment to the airways, it subsequently re-placed the need for cartilaginous support of air-ways lumens. The presence of cartilaginous ringssupporting thelumens of theelephants extra-pul-monary bronchi and trachea demonstrates that

elephants are indeed capable of developing suchairway support structures.

Acknowledgements

We thank Professor K urt Benirschke for intro-ducing us to this interesting problem, for hisencouragement and for discussion of the ideaspresented here. Discussions with Drs Fred Hop-pin and J ere M ead led to some of the ideas

presented here. We thank Bruce Ekstein, ToriHatch and Bonnie M eek for their efforts in thepreparation of the figures. We greatly appreciatethe opportunity extended by the Wildlife Safarianimal park, Roseberg, Oregon to attend thenecropsy of their elephant. Dr J ack M ortensonand Amanda Sallon of Wildlife Safari and thenecropsy team from the Oregon State University,College of Veterinary M edicine led by Dr OlafHedstrom were most supportiveof our efforts. DrGeorge K ennedy of the College of VeterinaryM edicine, K ansas State University generouslysupplied the domestic animal lung tissues. Thiswork was supported by theBeth Israel AnesthesiaFoundation and H L 52586.

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