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Rate and character of the compensatory renal hypertrophy after unilateral nephrectomy in young albino rats.

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KATE AXD CHARACTER O F THE COMPENSATORY
RII:NAL HYPERTROPHY AFTER UNLATERAI,
NET’HRECTOMY Ih’ YOVKG ALBISO RATS
C. M. JACKSON AXD S. hf. LEVINE
I n s t i t u t c of Anatomy, Universitjl of Xiiiiiesota, Mmricapo1i.s
TV-0 FIGURES
Various: investigators (11o w l iiiicl Verliac, Canlot, Hiiiman) have fouiid after unilateral nep1irectom;v a rapid enlargement of the remaining kidney during the first week or
two following the operation in various animals. This preliminary enlargement, or pscudohvpertropliv, lias been ascribed to a sudden congestioii or increase in renal fluids,
m-hich sooii sullsides and is followed by the more gradual
increase in reiial weight, representing the true compensatory
renal hypertrophy. Fiori ( ’01) and Smith and Noise ( T i ) ,
however, observed in adult animals a progressive increase in
compensatory renal liypertrophy, with no rapid initial enlargement. Jackson and Shiels ( ’ 2 i ) likewise found no inclication of this preliminary pseudo1i~~pertroph~after unilateral nephrectomy in young albino rats, but they did not
study the clianges during the fiwt week after tlic opcrntion.
The present experiment was therefore undertaken to cletermine whether there is an initial period of rapid or transient
increase in renal weight following uiiilateral nephrectomy in
:-oung rats aiicl also whether tlicrc are any sigiiificaiit changes
in the water content of the kidneys cluring the experiment.
~TATERIATJAND JIETIIOIIS
The albiiio rats (Mus iiorvegiciis albinus) used in the esperiment were reared in the colony at the Institute of
323
Xnatomg, from stock originally obt.ained at Tlic T7ista.r
Iiist.itut,e of A.iiatomy, Philadelphia. Tlic diet was a mixtwo
of onsein 15 per cent, whole-milk powder 1.0, sodium chloride
0.8, calcium carbonate 1.5,but,ter 5.2, .whole wheat8 (ground)
(ii.5. .Wtttcr was givcii a.d libitum.
Seven litters were used including fort.y-two rats (in adclition to t.lirec rat.s which were later escludecl because of
h ylr on epli r osi s ) , t.weiit,y males and t,ven t.? -two f e.malcs. ‘L’h e
sexes, and the litters so fa.r as possible, were divided eqiiallg
bet~wecn t.he t.c?st.and control groups in pairs which were
similar. also in body weight.
The operations mere performed Rlien the rats wei-e twentyc . b i g l i t days old (iii two cases at, tliirtT; ( l a . y ) ,whitdl was aliont
ii week after xveaning. Iii {lie t;est riits the operation lvas a
right-sided nephrect.omy by limhar incision unt-ler ether
anest.liesia. Followiiig exposure, the fibrous capsule of thc
kitlaey \viiS incised aiitl i*e.t.r;tctetlover tlic pc:dic.le, mhicli w w
ligated. ‘l’he pcdiclc was then cwt. clist.al t.o thc 1igat.in-c%
aiitl
the kidiie;v wa.s rcmoced. The luml>ar muscles and skin w i * e
s ti t 11 red stqx.~
rat el?, arid c.ollotlioii TWS applkd to p 1+otcxt tlw
~v0~111d. Tho control ri1t.s were similarly siihjected t o tlic
ct her ancstliesia, lumbar incision, and exposure of the liitlnc!y,
i.t.., t.o 11ie same cxpcrimontal procedure as in the test ixts,
osccpt.ing the removal of t.lie right kidney in the 1.at.t.w(base.
Al’lcrr t.ho operations, both test. aiitl ~oiit.~=ol
rats recovered
1)rornptly and wcrc r.etiirned to t i c k c ~ g e s . Tlicy coiititincyl
‘lipon t,hc same diet as before, ancl the wounds Eiealed in a few
(lays. The rats T\WP weighed iiidividnal1;v everp day.
I l l ortler to fit11dy tl:N? progl~essof tho r e n d 11ypertrophy,
1 1 i ( h rat;s, both the test ;inimals ancl the wrresponding ccmtrols,
\ v ( w killed by ethcr. One pair mas killed each day np to
t ! o ~ ~ ~ t dil:\Ts,
~ > ( i i ;111t2
~
t l l ~ r e a f t tC’:.V(II’Y
~ ~ ~ ~s<~+oild
( l i l y 111) t o t \ \ ~ t ~ i l l ~ (lixlit days after the opcr.R t’1011.
At i I i 1 t O f ) S y lhe 1Vo1111tl alY% alld tile viscctra \vel’c? cii1l.c.f1111~
c ~ s ~ n i i i t ! r l . ,111 gciicral, the\. appeared iiormal, c>sc*eptiiigovc.asiona1 adlicsioiis of t.he liver or intestine in tlic wpion of
original i.ncision. A s a1)ove mentioned, t1ii.c.e WRCS w t ~ e
o S ( ~ l i i t l ~ cf’iwn
1
t lie wr.i(?soil ;ic.couiit of! li~tTr.oiic.~~~11i~osis.
tli(1
After gross examination and wcighiiig, the kidncj-s vere i.n
some (~ases(one of t h o kidneys in cadi conlrol rat and in
overp second test rat.) c.ut transvcrscly in halves with a razor,
one part being fixed in 10 pcr cent f o r m a h for microscopic
study, t.hc other part being used for drying. In the other
cases the eiit.ire kidney was uscd for drying. There was no
tipparent difference in the water cont.eiit, whether t.he half or
the whole kidney was used. 'To determine t,lie dry weights
(and water content,), the kidneys were dried for three weeks
or more to const.a.nt weight. in open weighing bottles, kept in
an elect.rically heated oven at 95" t.o 100°C. I n a few cases
t.he dried kidneys were lost through accident.-which explains
the blanks in table 1. Frozen sections were made of the
formalin-hardened material, and were st.ainec1 with hematoxpliii-eosin (in some cases wit.11 sc.arlot .rcil) to determine
whether the kidneys were entirely normal in structure.
BODY WEIGHT
Figure 1 shouys the average body weight of thrt test and
eoiitrol groups of rats during the experiment, in comparison
: I ~corresponding
i~i~)
wit.11 t.lie Wistar iiorm ( ~ o i i a l ~ ~ s o r ~ -for
age. The number of rats in each of these groups decreases
progressively from twenty-one 011 the first day to one on the
twenty-eighth day, when t,he last pair was killed. The average body weight in t.lie test group inc.reascd but. slightly (0.7
griim) on thct first da7- a.fter the operation, hiit thereafter tlicr
growth was remarkably regular. l!he coiit rol group (subject.ed to operation, but without removing the kidney) inc?i:eased stcadily from the beginning, and their gro\vth cur\-(?
t.lirougliout rcmaiiied remarkably close t.o that. of the tost
group. I n general, the average body weight increased from
ahoul 58 grams a t the heginning to 200 grams in tlic test rats
and 188 grams in the controls at tlic end of tlic cspeyimerit.
T t is evident. that. in h s r ? young rats the operation, either
wit11 or withoiit removing one kidney, did not. apprcciahly inI-errnpt the growth in hod^? weight. I n adult rats, 011 the
( . ~ trar?-,
ii
Smith ant1 3Ioisc ( '27) noted following unilateral
326
C. M. JACKSOF AND N. M. LEVINE
COMPEKSATORY RENAL HYPERTROPIIY IN RATS
327
nephrcctomp a loss in bod;\- weight, wliicli was not regained
until after two to four weeks.
I n comparison with tlie Wistar norm (Donaldsori’s chart
21, for King’s data), it is furthermore clear that in the present series the hody weight was about one-third above the
normal for age at the beginning of the experiment. The
subsequent growth was also above the normal rate, so that
the rats (both tests and controls) were about 50 per cent
above normal weight toward tlic end of the experiment, as
slio~vnin figure 1.
sE Y w EIGI i r r
Fresh weights
In control rats, as sliowii in figurc 2, the weights of the
right and left kidlie? in each rat were closcly alike, although
the right was usually slightly heavier. The average excess
of the right kidney was 3.94 per ~ e i i f ,which is in general
agreement with the findings of Jackson (’25) and Arataki
(’26). It is remarkable that during the first six days therc
was apparently no significant change in the kidney weights
of the control rats. This retardation was probably caused
bp the operation, especially the anesthetic, although it did not
prevent an iiicrease in hody weighl, as above mentioned, during the corrcsponding period.
In the tcst rats (fig.2) tlie average wtlight of the twenty-one
riglit kidneys, remored at operation, was 0.384 gram. We
may assume that the corrcspoucling average initial weight of
tlie left kidney was about 4 per cent less, or 0.369 gram. In
tlie test rat killed one clap aftcr the removal of the riglit
kidney, the remaining kidlie:- showed practically tlie same
Iveight as the left kidney of the control. Tliercaftcr, tlie lcft
liidney showed a variably progressive liypertroph;v, in comparison with tlir left kicliicy i n the coiitrol rat of the same age.
There is e~ideiit1:- some irregularity due to individual variations (especially on tlicl iiiiitli a i d eighteenth clays), but
aftcr thc first week there is a remarkable correspondence in
tlic incrcascs and decreases of liidiiey n-eight in corrcsponding test and control rats,
KII
328
(1.
M. JACKSON ANI) N. AT. LEVINE
329
COXPENSATORY RENAL HYPERTROPHY ISr IL4TS
As shown by the growth curve in figure 2, the hypertrophied
kidney apparently increased rapidly in weight during the first
three days, lout decreased somewhat during the remainder of
the first week. During the second week the kidney agaiii
showed a marked increase in weight which continued somewhat irregularly through the third and fourth weeks of the
experiment. The percentage hypertrophy of the kidney was
slightly more irregular, as shown in the second column of
table 1. However, there was apparently a rapid incwase to
TABLE 1
Prrcmtnge hypertrop7q ir .iCeight of the left kidn.ny ( f w s l r tiwight, c o m p r e d rait7t
Zeft control) and percewtage of dru sztbstance an each kid?t.ey at sari.oti.r
dnjls following Ike operation
..........
I’BRCENTAQP
.
.
DAYS
,HYPERTaOPWYi . . ~.
FOLLOWIScl
OF LEFT
OI’ER.A’I’ION
XIDNBY
li 111
9f
10 f
11f
12 m
13 f
14f
16m
18 ni
‘70 m
20 ni
24 ni
26 m
28 in
26.02
63.98
44.78
47.67
50.64
46.44
49.25
43.94
80.80
35.06
73.97
41.56
61.02
58.60
....
I
3lcan
Standard deviation
Prohable error
. . . . . .
’
OF D R Y SUBSTANCE IN KIDNEY
............ ........
In teRt rats
Kight removed
a t operation
0.40
26.61
34.89
12.90
28.63
23.19
... .
’
.’
If
2f
3 111
4f
3f
6f
if
~
I’EROENTA(2E
~
90.36
18.52
90 1 2
19.85
--.
....
21.85
30.65
19.79
19.56
In control rat>
Left removed , Ltieht removed
at autopsy
i i t autopsy
21.18
21.91
19.51
22.68
21.41
....
....
....
02.46
20.58
21.42
31.78
20.92
21.16
00.18
20.95
31.87
21.10
‘30.44
20.98
‘70.12
22.09
20.51
22.89
“0.55
19.64
19.54
22.50
21.90
22.49
23.70
22.64
02.;2
20.83
0.963
0.1 3
21.52
1.24
0.1 0
....
20.33
0 : ) 98
18.97
--.A
’
21.68
20.93
21.38
19.37
21.18
20.54
21.51
21.59
21.87
21.51
00.40
19.06
21.08
Left removed
at uutops~
212T
22.78
21 .i6
20.86
....
31.46
19.84
19.90
22.19
20.90
22.02
21.24
22.18
21.76
20.32
19.6i
03.08
21.i9
21.73
22.62
22.89
03.33
’71.14
1 .12
21.52
1.01
0.1 i
11.13
99 58
--.
22.28
....
330
C. M. JACKSON
A N D N. AT. LEJ’IXE
about 35 per ceiit hypcrtropliy at the end of the third day,
thcii decreasing to a lower level, beiiig about 13 per cent 011
tile fourth clay. Thereafter, tlie percentage hypertrophy increased irregularly throughout the period of the experiment.
The filial hypertrophy a t the end of the fourth week was
ttl)ont 60 per cent. Tf Donaldson’s norm (for kidneys at
c~orr.csI)oncJiii~
body weight ) ~ v e mused for comparison instead of the Control left Bidiieyvs, the apparent reiial Iiypertrophy wonld be much greater, 1)ecause the control kidneys
iii-c Ihemselves somewhat ahove Donaldson’s norm.
‘l’lie results of the presciit experiment are thus in general
agrccment with the theory of an early period of pscudohypert ropliy (congestion), followed by subsidence aiid snhsequcnl
i)iwgi-essivetrue reiial hypertrophy. However, a larger iium1 ~ of1 C ~~S C ‘ S , cisprcially (hriiig the first week, would lie nccess;i i’y to ~stnhlislithis conclusion with certainty. The present
rwult might possibly he due merely to chalice variation among
t h e rclativc1~-few individuals.
Ur?y z(*rigl(tsa d u - a t w cordelit
A s slioivii iii table 1,tlie dry substance in the normal riglit
kitliiey (wmoved at operation) of the test rats averaged
20.83 .I> pcr ccwt. 111 the wmaiiiing liypertropliicd left
kichey, rcmowtl latw a t autopsy, tlic dry substance averaged
2 1 X 2 .19 per cciit, or 0.69 per cent greater. The probal~le
t w o r of ilie cliffcrence of the two means (obtained I)y taking
t 1 1 ~square root of tlie sum of their probable errors sqnarccl)
is 0.24 p w cent; so that the cliffercnce, being slightly less
t h i i three times the probable error of the diffcrence, is of
cloiihtfnl sigiiificaiicci. A slight relatirc increase in dry sn1)~ t : ~ i i of
( ~ tlic. ltitlne>v with agc might l ~ c i cspectccl n o ~ m a l l y
( h t w Lo1\-1*e~’h datii, cited by T)onaldson).
‘Po detc.i-mine wlidher there has been aiiy cliaigc i n the
water coittciit of tlic kidney as a result of tlie compcwsatory
liypcrtroI)h~-,the hest comparisoit is l)ctwccii the hypert 1-opliicdleft kidney of tlic test rats aiid the normal kidney of
t h c control rats of the s a i i i ~agc aiid bod- weight. As is
COMPENSATOBY XENAL HYPERTROPHY IX RATS
331
apparent from table 1,tlic! mean relative dry weight in the left
control kidney was 21.52 per cent, o r exactly the same as in
the hypertrophied test kidney, while that in the right control
(21.14 per cent) is not significantly different. Therefore, the
conclusion is that there has been no significant change in the
relative dry substance (or water content) of the hypertrophied left kidneys of the test rats.
Since there is no marked change in the water content of
the hypertrophied kidneys, it is clear that the increased
weight could not be due merely to an increased amount of
water or watery liquid (such as urine) containing very little
solids. This is confirmed by the microscopic study of the sections, which show no indication of edema or dilatation of the
uriniferous tubules. Smith and Moise ( '27) found a definite
increase in the relative water content of the rat's kidney during late stages of compensatory hypertrophy on high-protein
diet, but not much change during the earlier stages. They
record no observations for the water content on normal diet.
Cameron and Kellaway ('27) found no appreciable increase
in the water content of the hypertrophied kidney in young
guinea-pigs after unilateral nephrectomy or ureteral ligation.
The lack of any definite change in the water content of
the hypertrophied kidneys in the present series might be
thought to exclude also the possibility of a renal hyperemia,
but such is not the case. Donaldson's data for the water
content of the rat's blood indicate that it is only about 2 per
cent above that of the kidney at body weights corresponding
to those of the present experiment. It therefore follows that
an increase in blood sufficient to raise the renal weight onethird would increase the relative renal water content only
about 0.66 per cent, which would appear insignificant in the
present series.
No detailed histological study was made of the kidnevs in
this series. Hyperemia was frequently observed in the sections, however, in agreement with the observations of Albarran ( '99) and Saphir ('27). Jackson and Shiels ('27) observed no excessive renal hyperemia, hut their series did not
iiiclude the first week following the iiephrectomy. Since,
furtlieimore, it is very unlikely that any coiisitlerablc amouii t
of trnc cellulai*growl 11 coiild occ~xrn-itliiii three days, the (*oilclusion seems justified that the early iiicreased reiial weight
following nnilateral nephrectomy is a pscudoliypertrophy t o
I M ~ ascribed chiefly to blood-vascnlai- congestion.
s u M3I.Aa 1-
1. The right kidney
TWS
removctl in twciity-oiic alhiiio rats
at t wciit.y-eight, clays of age. Tweiit.>--oiielitter-mate coiit.rols
to the same operation (anesthetic, incisions,
.ant. removing the kidney. The subsequent
gro1vth in body weight was not apprec.iably retarded by the
o p r a t i o n eithei. with or wit)hont ricphrectomy.
2. T e s t rats aiicl .corresponding coiitrols were killed and
il nt opsiecl at. succ.ess.ive int.ervals, tlailp up to fourteen days
a i i t l every secoiitl clay thereafter 111) to t,wenty-eiglit i l a ~ - s
ii f t c’ L‘ ope rat.ion. The operat ion u7it.h anest.1iesi.a apparent.ly
piwwitecl the iiormd growth of t.lie kidney during the first
1vec.k in tlie c.ontrol rats, although tlic growth iii bod^ wciglit
wiis nnaffectcd. Aft.er the first week, the gr0wt.h of the kidnc:\i i i the cwiitrol mtx appeared normal.
TI141 right control
Ititlney avcmgetl ahout 1 per cent. heavier tliaii tlie left.
3. In the test i*cit.sthe rema.iriiiip left kidiiey t i t first. incwawtl rnpidl~7in. 11 glit, reaching an apparent 1iypc:rt i ~ ) p l i ~ of a l ~ o u t35 per cent in 1.hree taps. ,4 clecreaw in reiial
wciglit appeared during the remainder of the first .week.
Siil,scrii-lentl,1~,tliere was i i n irregiilaialy I)rogi*cs.;Si\.oi~ctnal
Iiypcrtroph-y, finally rcvwliing ahoiit. 60 per ceiit.
4. The dry weig1Jt.s showed no sigiiific.aiit differences i n
i*dat-ivcnatcv contcn t: of t,lic hypertrophied left Ititlneys, i ti
c.omptirisoii with either tlic normal riglit: kidiieys of the test
rats (removccl a t operation) or tlic kidneys of the control
rats of‘ the same age and hodp weight-.
5. The lack of any apprccia1)le cha.iigc! iu relative matt?^.
twiiteiit of the li-r)c!rtI.oplii(!(l kirlncys, as w-cll a s tlic histo1o gi cal appearance, (!wl iitlcs t 11 1 )ossi 1) i 1it y t 11ii t. tli i iic rea R W 1
(1
(1
reiial weight might be h e to iiicreasctl content of urine or
other liquid of low solid content. This does not, however,
exclude the presence of a marked hyperemia, since the relatire water content of the blood is bnt slightly above that of
the kidney.
ti. The results are therefore in agreement with ttic tlieoqthat, following unilateral nephrectomy, there is an initial
transient psendohypertropliy of the kidiie:-, t h e chiefly to
hlood-vascular congestion, wliicli suhsicles arid is followed by
progressive true rciial hypertrophy. To establish this conclusion with certainty, however, a larger unmhei. of cases is
nccessiarj-, especially &iring tlic first ~ w e k .
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young, albina, character, nephrectomy, renar, rate, compensatory, hypertrophic, unilateral, rats
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