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The growth in surface area of the human gastric mucosa.

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The demand f o r ail accurate knowledge of the structure of
the stomach during the growth period is evidenced 1)y tlie
publication of many papers on the subject. At the present
tjme tlie qualitative clia'nges in the various layers of the
stomach wall are moderately well described. There are considerable published data available on the ponderal and capacity growth in this viscus, aiicl its position and anatomic
relations, at all ages, have been described in the literature.
The dimensional and numerical growth of the crypts and
glands has heen considered t o a certain degree. That the
growth changes in surface area of the mucous membrane
have been neglected is not astonishing. The many difficulties
which attend the pursuance of such an investigation are
obvious. Yet such knowledge is of considerable importance
in estahlishing the anatomic norm, at various ages, for this
In connection with a study of the growth of the crypts and
glands of the human stomach (Scott, '23) it was necessary to
arrive at an estimate of the surface area of the gastric
mucosa. The observations made in this investigation and
in a later quantitative study of the developmental changes
in the wall of the liuman stomach (Scott, '29) hronght to
'This study was aided by a grant f r o m the Fenger Meriiorial Association.
light points of such interest that it was decided to make
furtlier observations upon the growth changes in the area
of tlie gastric mucous membrane. I n addition, it was deemed
advisable to attempt to influence experimentally, if at all
possihle, this surface of the stomach.
The technical difficulties met with in such an investigation
are many. First and probably tlie greatest of these is procuring material which has iiot become macerated. Unless one
Iias a(*cess to such a mass of material that the most rigid
selection may be exercised ~vithoutfear of completely disrupting the continuity of the series, it hecomes difficult, to
obtain suitable specimeiis for examination. I n the arailable
literature there is recorded a relatively small number of
measurements of the gastric mucosal area. Toldt ('80)
tletermined the area of the mucous membrane of the stomach
in a series of fire individuals ranging in age from the eighth
fctal month to fifteen years. Dargein ('99) made a comparison of the mucosal area of the stomach and duodenum in
twenty-two adults and of seven infants in the first pear of
life. Lissenko ('99) calculated the surface area of the gastric
miicosa in a series of seven humans of different ages.
With the generous cooperation of the Department of
Pathology of the University of Minnesota and of the Children *s Bureau of the Department of Labor, Washington,
1.. C'., under the direction of Dr. F. L. Adair, it was possible
to have access to a large iiumber of stomachs taken from
iiecropsied infants and children. This abundance of material
made it possible to collect a sizable series of suitable organs
in the course of three years' time.
Another technical difficulty that was encountered was the
devising of a method for the determination of the mucosal
area which was a t the same time workable and productive of
reasonably uniform results. The method used by Toldt ( 'SO)
consisted of spreading the fixed and hardened stomach flat
upon a glass plate and outlining the area covered. The area
in square centimeters was then determined with the Amsler
planimeter. This method does not take into account the
very small folds and surface irregnlnrities of tbc miieosa.
Dargeiii ('99) nsed a. wreak solution of acid to macerate the
stomach and then removed the mucosa in pieces. Afterward,
the bits of mucous membrane were placed on squared paper
and the approximate integration method made use of in ascertaining the area covered. Tlic errors introduced by these
methods of determining irregular areas in morphological
studies have been pointed out by Scammon and Scott ( '27).
The results thus obtained hy the several authors are at
considerable variance. This is probably due in part to the
very divergent tecl~niqiiesemployed. The differences of the
mucosal area of the newborn hnmaii stomach, as determined
by the rarious workers, map be taken as a fair example of
these cliscrepancics. These figures range from 12.75
(Dargein, '99) to 52.7 (Toldf, '80). These data ham
heen summarized and depicted graphically by Scammoii ( '19)
a11d by Scott .( '25).
The material nsed hi this study consisted of ninety-six
stomachs from individuals ranging in age from six fetal
months to fifty years. The stomachs were obtained as soon
after death as was possible. In no case was t.he elapsed time
between death and fixation greater than four and one-half
hours, and in a number of cases it was one hour or less.
Specimens which showed marked contraction or dilatation
were rejected from the series. The weights of the stomachs
were compared with the data of Scammon ( '19). Those
which showed any marked variation (more than 100 per cent)
from the mean weight for the stated age were discarded.
Every attempt was made to secure only those organs which
were normal. Full recognition was given to the fact that
the stomach is a highly variable organ in both weight and
The estimates of the ages of these specimens were made
with the aid of the empirical formulas for determining fetal
age developed by Scammon and Calkins ( '23).
‘L’he stomachs were fixed as soon after removal from the
lmclj- as practicable. In erery cast1 tlic stomachs were filled
with the fixing fluid (Zenker-acetic) and immersed in a dish
containing tlie same mixture. After fixation f o r twenty-four
hoars, they were washed in riinniiig water for a n equal length
of time, transferred to 50 per cent alcohol for three hours,
il1lcl placed in 70 per cent alcohol.
, W e r the specimens had liardened in alcohol f o r three days,
the? were ~ ~ e m o v e dsplit
in halves by incisions along the
g w a t e i - and Icsspr curvatures, and a plaster cast made of the
miicmal surface. This was done by pouring a 20 per cent
soliltion of glycerin over the stomach and then pouring into
tlie \-eiituicular cavity a paste of quick-setting, non-shrinking
1)lastt.r of Paris. The cast mas removed from the stomach
aiicl allowed to dry.
As woii as tlie plaster of P a r i s was sufficiently dry, thiii
tissiich lxtper. was moistened a i d fitted carefully over all of
tlic hurfaee irregularities of the cast. This paper mas allowed
to clry in position, carefully removed, and spread out upon
standard-weight paper (Resolute Ledger no. 3 2 ) . The outlines of the tissue paper were marked and the covered area
cut out witli sharply pointed scissors. This paper was then
weighed. The weight of the outlined paper being determined
iIlld the weight per square centimeter being known, it was a
simple matter to rcduce it to terms of square centiineters and
a r r i r e thus indirectly at a n estimate of the area of the gastric
miicosa in terms of the same unit of measurement.
T o test the accuracy of this method, the area of one stomach
was determined twenty times. The area of this stomach, that
of a nev-born infant, was 32.13 The probable error of
tlic twenty observations was i- 0.38 The standard
dcviation was 1.37, with a probable error of 4 0.12, and tlie
coefficient of variability was 1.02 per cent. It will be seen
from this set of observations on a single stomach that the
method is proclnctive of reasonably accurate results.
I n a fetus of six moiiths, calculated age, the surface area
of the gastric mucosa averages 9.65 sqxm., with a probable
error of fr: 0.21. The variability at this age is small, as
indicated by the standard deviation of 0.435 and a
coefficient of variability of 4.51 per cent. By the seventh fetal
month this value has increased approximately twofold and is
now 18.16 sqxm., with a probable error of + 0.10. The rariability is even less than in the preceding lunar month. I n
the following two fetal months, the eighth and ninth, the
increase in surface area of the gastric mucosa is steady and
relatively slower. By the eighth prenatal month it has attained 23.75 and in the succeeding month has reached
27.20 I n the tenth fetal month there is an average
increase of practically one-third of its former value, so that
by this time the mucosal area is 36.93 The variability
has increased in proportion t o the rate of growth and its
coefficient at this age is 20.92 per cent.
At birth the area of the mucosa in square centimeters is
39.17, with a probable error of t- 1.36. The coefficient of
variability is at this time 24.68 per cent and represents the
highest variability of any group of the series. This may be
explained by the fact that a part of this class were stillborn
infants and a part had lived f o r some varying lengths of
time. I n some instances the infants had lived f o r several
days and had undoubtedly taken food. It has been shown by
Scammon ('19) that the stomach increases in capacity very
markedly in the first weeks of life. That this is an actual
growth rather than an adjustment in muscle tonicity is shown
by the members of this series which had lived and ingested
food. Invariably, these specimeiis exhibited greater mucosal
areas than the stillborn infants. This fact is also emphasized
by the increase in stomach weight in early postnatal life.
The frequency curve given in figure 1 illustrates the distribution of the observations on the neonatal series.
Although the selectioii of material for this group was made
d o i g very rigid liiics, oiie could iiot jnstifiahly iiicliitle 011ly
sti1ll)orn infants. The maiiy factors wliicli may iiifiueiice
stomach growth make themselves apparent in the iieoiiatal
material presented in this series. The tu-eiity-three cases
giveii in table 1were selected from a group of over 150 speci-
Fig. 1 A poilit-to-point freyuoicy c u r r e of the tlistrilmtion of the 01~scrr:itions
tlie surf:ice aw:i of tlicx g i s t r i c iiiucosa ill tlie newborn infant. A l d s s a s :
nui1iIicr of c:ises in r:rcli class.
0rtliii:ites : c*l:iss groupings i n terms of square
t iiucters.
were collected and examined. Tlie most of these
\\-ei*e rejected because of postmoi*tern cliaiigcs o r tlcfiiiite
pntliological findings.
I'OSt ?I ntnl
The postiiatal material was groupetl in table 1 awordiiig
t o tlici number of specimcus collected for a given time leiigtli.
I t i v a s o1)vionslj- impossible t o secure an eveii tlistribntioii
of matcrial in a study of this sort. The relatively small
number of cases given was selected from considerably over
4-00 stomachs collected. All specimens in which definite or
suspected gastro-intestinal lesions were demonstrable were
rejected. Stomachs from persons dying of diseases with
which gastro-intestinal disturbances arc associated were
6 fetnl moutlis
7 fetal molltlls
8 fetal mouths
9 fetnl moutlis
10 fctril montlis
0- 3 montlis
3- 6montlis
6-12 nloiitshs
1- 2years
1- 4 years
4- 7 yell3
7-14 Y W ~ S
20-60 pears
9.G5 f 02
13.75 f 0.91
27.20 f ]..A8
36.93 -t 1.6.5
39.17 2 1.36
1.28.69 2 7.07
169.58 f2.17
174.58 f3.15
248.06 23.73
236.40 2 6.90
263.69 k 2.64
329.31 f2.03
525.88 zk 5.7G
2 0.15
f 0.07
2 0.64
Per cent
f 1.12
f 1.16
-C 3.37
2 2.23
f 2.64
f 4.88
f 0.47
I .n9
IIn several of tho age groups the number of ensea is too small to lcud siguificance to the statistical nierisuree employed, but they were applied to the data
for thc sake of uniformity.
In the group aged from birth to threc months the surface
area of the gastric mucosa is 128.69, or over three times
its value a t birth. The probable error is 2 '7.07 and the
coefficient of variability is 15.53 per cent, or approximately
10 pcr cent less than at birth. By six moiitlis the mucosal
area has increased to 159.58 and by the end of the first
year of life it has attaiiied 174.52 I n the first ycar
of lifc the surface area of the gastric mucosa has increased
fourfold. In the succeeding ycar the rate of growth has
become considerably retarded, for at the cnd of twenty-four
months the mean value is but 208.06, with a probable
error of 3.i3.
I11 the iicxt two years tlie growth in mucosal area of ilie
.stomach is but slight, f o r a t the fourth pear it was found to
1~ 235.40, with a probable error of r+ 6.90 and a coefficaicnt of variability of 13.75 per cent. From four to seven
!.ears represents ailother period of slow growth f o r this surface of the stomach. The mean value of tlie surface area
of the miicosn at this timcb is hut 263.69 111 the succeeditig sevm years therr=is an inertlase of about 6< for the
l\\-rragc of the pei.iod of seren to fourteen >-ears. At this tirnc
it is 229.31
k’ig. 2 fi siniple liistograril, tnkrn from the data in table -1, which illustmtt~s
the growth i>li:inges in t h e riiucosal a r e a of the stomacli.
The figiires given f o r tlic adult s t o m a c h a r c an average of
six specimens, four of Tvhicli were accidental deaths and the
r~rnaiiiiiigtwo were suicides by mercuric-bichloride poisoning. The age range is large, but no significant difference was
found in any one of the group. The range of the observations
u-as from 493.26 to 551.12 The mean value f o r this
group was 525.58 sqxm., with a prohable error of I
sqxm. a i d a coeficieilt of rariability of 4.59 per cent.
The data from which the above figures were taken a r e summarized and preseiitocl iii table 1 and illustrated graphically
by a simple histogram in figiire 2.
N i i i ~ i l w rof
f o l d iwrfiase it2
surface arca
of t h e gastl-ic mzicosa
By the simple expedient of dividing the mean area of the
mucosa in tlie adult series hy tlie mean d u e a t any selected
age, the result is the number of times which the area has
increased betwecii a givc~iiage and matnrity. These figures
are t o be found in thc last column of table 1. T t will be seen
that the surface area of the gastric miicosa increases 54.46
times betwemi tlie sixth fetal month and maturity. By the
next fetal moiitli this d u e has dropped to 28.94 times and
decreases steadily thereafter iiiitil birth. From birth to maturity the mncosal area increases but 13.42-fold. After the
sudden drop in the number of fold increase j i i surface area
in the first three moiitlis of life, there is a slow steady
decrease until the adult stage is attained.
These figures sliosv clearly the periods of most rapid growth
in mucosal area of the stomach a s represented iii the preseiit
series. Obaio11sly, the most rapid growth rate is bet~veen
birth and the third month of life. There i s aiiotlier period
of accelerated developmelit between the sixth aiid sereiith
fetal months. At other times during development, p r t i c u larly postnatal growth, the i n c ~ e a s ein mucosal area is slow
and even. I n the prenatal series tlie same steady course of
eiilargement is followed, but it is more rapid tliaii that which
i s foiiiid after birth.
E f w t s of distPiitiou
gust r i c
tlir S I . I Y . ~ U ( Oc l r m of t h c
Tt was ilecidetl to test c~xperinieiitdlytlic efiects of marked
t~s-pansioiiupon tlie surface area of the mucosa. The technical
difficulties n.hic.11 p ~ ~ c s ~ ~tliemsclvcs
obviatccl any attempts at direct measjliwmeiits of the rcwilts. The fact
that it u7as impossible to amirately determine tlie mucosal
area of a stomach contracted aiid later measnre the samci
area of the same stomach when distended made it necessary
to draw upoii inferential evideiice to aid iii tlie solution of
this proldem.
Frcsli ncw-boni liuinaii stomaclis wercl distended with fixing
Auid at cliff creiit pressures. The pressure in each stoniacli
W ~ Skcpt constant foi- a period of ten hours and recorded
mcaiirvhile with a mei*cury manometer. After the stomach
had tlioronglily hardcnecl, pieces n % r ~cut from each of tlic
sevei*alparts and prepared f o r sectioning. The sections ~ ~ e r c
stained witli liaematoxylin and cosiii. Whcn compared with
swtioiis of corrqmii(1iiig ])arts of normal and undistendcd
stomachs, they rcv-calecl but little cliarige in the thicbiiess 01
1 lie mncosa and g e n c i d histologic: appearance. 7’he musclc
laycrs m’re tliiiiiietl somewhat and the submucosa was flattcwctl. TV4ieii the pi-c~ssurc~
was over 200 mni. of mercury,
tlicrci was a cliange iii tlic mncoc;al layer. Tlie crypts WC~I’C
shortened, and wh~11tlic pressnre amounted to as much as
250 to 3OU mm. of Iyi(’i*ciiry,cr.acl;s appeared in tlie epithelium.
of tlisf(~iitioiiupon thcl newFigurc 3 illustrattbs tlir e
Imrn infant’s stomach. In
first figure, u,tlie mucosa is
indicated by solid 1)lacB. This figure exliihits tlic typical
histologic appearaiice of the normal nen-born in
sttrmavli. 7’he secoittl figure, 0, is a stomach from il specim ’ i i of the same cJalculatcc1 age, wliich was distmdecl at ii
uro of 120 rnin. of mrrcwry. Tllere is n o cvideiicc of
Iiangc i n the miwosal layer aiid but very slight d t e r a tioii i n thc sihmucosul aricl niusclc layers. In tlie last figure,
I , tlic pictirrcd js tlint ttf a iiex1)oi~n
iiifaiit. The
1)rcssure of disteiitiou in this instance was 2%) mm. of
n i c ~ r (ry.
~ i The ~~pitlic~liurn
s1iou-s 110 evitlence of flatteiiing, the
rypt h
s o m e d 1 a t short enecl, and t 11e g.1and s a IF likewise
K ~ O U ’I)lunt tlian tliow ovdiiiarily seeii in the untlisteudecl
b i ornacli.
The miisc~le1ayei.s arc considerably flattened aiitl
hi~iiclles more scparatotl. ‘L’liis is also true of the
Fig. 3 A wi ies of figuivs ill i i
trlig the effects of distrrition iipoii t h t .
~ i c ~ w l ) o i iiif:uit
’s stoni:rc*li. All figure3 weie i1r:iwii with the Edinger app:iratur
,it a stant1:irtl niaynificatioii. The epithelial parts of tlie inucosa are rcprcseiitml
111 soh(l blavk.
u, :I nnimil uiidistciided stoiiiacli; 11,
stomacli disteiidrd a t
1% in[ii. rrf riiei( [iry pressure: c, :I stoni:icli (listended a t :I picssuie of ?t‘O mrii.
of mriwry.
Figure 3
&Ill figures were drawn at a standard magnification and
from sections taken from corresponding parts of the st omaclis
this case, the corpus from the midventral portioii-ant1
at a~qxosimatelythe same location.
Tlic same experimtiiits \verc tried wit 11 the white-rat, rahhit,
vat, and clog stomaclis. These were distended in sitn in
;incstlietized aiiimals. Iii the c a s e of the rat stomachs, the
miicosa (lid iiot show evidence of thinning until pr
near to t h e h r s t i n g poiiit were used. The mean h
\troilgtli f o r the adult white-rat stomach was 127 mm. of
mcrcurj-. T l i c ~ e n’as 110 mwi*kcd x-ariatioii in himtiiig
streligtli, foi. the total range of ohsermtions was from 121
t o 13%
mm. of mercury. I n the rat the tear als\-nys took place
iii tliat portion of the wliich was lined with strntificd
hcpamou s epitbeliurn.
The rabbits’ stomachs gave esseiitially the same resnlts
a h ~ w r eol)taiaecl for the lien-horn Iiuman stomachs.
1)iirstiiig strength varietl from ICiO to 210 mm. of mercury.
‘i’lierci \vas little eriticiice of miicosal (*liaiige either iii sliortof’ c ~ y p t s01’ of thimiiig of tlie mwosal I a p r . Whc11
iires of approximatel:- 130 mm. of mercury ~vercircaclirtl,
t l w glnii(1s Iw+aine more compac+tly arranged than i n tlie
iioi*mally c~spandeclstomach.
\\-lieii vath’ stomaelis wci*e subjected to distention at 1)rws u i w var~-ingfrom 90 I(J150 mrn. of mercnry, a somewliaf
tljffcreiit cJfYcct was prodi~ced. Pressures 111) to 110 mm. of
rnc’rcury gave no cff’wt ul)on t l i c iniieosn. The glaiids rctxiiietf
ii c d . IT11a i hi pli e r 1)r e s 8111
w-ere attained, the glands
took the appearance of Iiaving been coiled upon tliemselrt+.
1’1it~ crypts almost tlisappearcd. ,Tohnson ( ’13) tlescrilwtl ;t
sirnilai. c+fect in this animal and also in the giiiiica-l)ig. H e
poiiitcd out tliut tliclrc is a sliorteiiiiig of both crFpt+ a i i t l
giaiids, wliic4i a t tlie same timc m w widelied a i d spwatl
a1)art. ;\Inller ( ’ l 5 ) , in a stiidy of tlie lmrstiiig strenptli of
t h e alirnviitai-y t r w l of the cat, states that tlie mucosa of
t l i c stomach which is ordiiiai*ily tlirow-n iiito rriai~y rugacl,
indicating EL considerable reserve for dilatation, reaches its
elastic limit very soon and tears. He found the mucosa to be
the layer which ruptured in advance of the submucosa and
The stomach of the dog is similar to that of the cat in its
reaction to hyperdistention. The glands become coiled and
the crypts very much shortened when a pressure of 150 mm.
of mercury is reached. The muscle layers a r e very much
thinned and the individual bundles a r e torn apart. Cracks
a r e present in the epithelium and in most cases the mucosa
is completely ruptured in one or more places.
It would seem from the experimental results obtained with
fresh newborn infants' stomachs and with the various aiiimals tried that normal distention of the stomach influences
but slightly, if a t all, the mucosal surface area. Until a very
marked degree of distention is experimentally produced,
there is no new surface presented by a shortening of the
crypts and glands. This is contrary to the findings of Johnson ('13) in the intestine of the cat and guinea-pig. H e found
flattening of the epithelial cells and a spreading out of the
villi coupled with shortening of the iiitestinaI glands. SlXCh
a happening would obviously present additional surf ace to
the lumen of the gut. This seems, however, not to be the
case in the stomach under normal conditions and, iii many
instances, under experimental pressures near to the bursting
The surface area of the gastric mucosa in man may be
measured with a reasonable degree of accuracy by means of
the method described.
The mucosal area increases 54.46-fold between the sixth
fetal month and maturity and 13.42-fold from birth to the
adult state. The most rapid rate of growth takes place in the
first three months of postnatal life, during which time it
increases over 100 per cent per month.
Sormal distention has little or no effcct upon the amount
of surface presented to the gastric cavity. Distention under
pressures iicm to tlie bursting strength results in an estension of the area of the mucosa which is evidently brought
about by shortening the crypts and glands. No change in
shape takes place in the epithelial cells themselves.
J)AWF.IN, 1’. 18!)!) Surface ct voliimc eoniptirk de I’estomac et du duodenuin.
Bibliog. Aiiat., vol. 7, p. 207.
F. P. 1913 The effrcts of distention of the jntcstine upon the. shape
of villi and glands. An]. Jour. Anat., vol. 14, no. 2, pp. 23&250.
LJSSESKO,W. 1899 The growt.11 and structure of the stomach in ehildhood.
Dissort., St. l’otcrsburg. (Quoted from review in Jahresb. f. Anrt.,
Bd. 3, 1900, and from Gundobin, A. P., 1912, Die Besonderheiten dcs
Kindcsalters, 8. 264. Berlin.)
II. R. 1915 Kottrr on tlie biirsting strength of the alimentarF tract
of the cat. Antit,. Hee., vol. 10, no. 2, pp. 5345.
It. E. 1919 Some graphs and tables illustrating the grort.11 of tlic
liumnn stomach. Am. Jour. Dis. Child., vol. 17, p. 395.
Sr.4nmox, R. E., AND CA~KINS,I,. A. 192.3 Simple empirical formulae for
expressing the lineal growth of the human fetus. Proc. Soc. Exp.
Biol. :md Md.,vol. 20, pp. 35.3456.
f+’AMJrON, R..E.,AND S c m , ti. 14. 1927 The technique of determining irregular
areas in morphological studies. Anrt. Ree., vol. 35, no. 3, pp. 269-277.
&-om, G. H. 1925 Growth of crypts and glands of the human stomach. Am.
Jour. Dis. Child., vol. 30, pp. 147-175.
1929 A quantitative study of the fetal growth changes of the
parts of the huinwn stomach wall. Am. .Tour. Anat., vol. 44, pp. 1-46.
C. 1880 Die Entwickelung untl Ausbildung der Driisen (1- Mngens.
Sitz. d. k. Ahid. der Wisscnsch. Wien., Bd. 82, S. G.7-128.
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