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An Experimental Study of Injuries of the Kidney1
AN EXPERIMENTAL STUDY OF INJURIES OF THE KIDNEY1 W. CALHOUN STIRLING
AND
A. M. LANDS
Front the Departments of Urology and Physiology, Georgetown University School of Medicine, Washing/on, D. C.
This experimental study of in juries of the kidney was undertaken: (1) to classify more exactly the type of injury produced, (2) to determine the response of the kidney to injury in both untreated animals and in animals following surgical repair, and (3) to determine the diagnostic value of pyelography in such conditions. Kuster was one of the first investigators to make an experimental study of the factors involved in kidney rupture, his investigations being made on necropsy specimens. The studies here reported were made (with the exception of a few cases) on the intact organ. Tuffier divided injuries of the kidney into three groups, i.e., ecchymosis, subcapsular rupture and total rupture. On the basis of some preliminary studies, we came to the conclusion that this classification was inadequate and that the nature of the reparative response of the kidney to injury should receive further experimental study. Lowsley described the effect on the kidney of instrumental trauma. We have been able to confirm his findings in part and these will be discussed later. This study was undertaken to determine what actually occurred in such injuries. In a series of 40 experimental animals (cats and dogs) we subjected the kidneys to various degrees of trauma. In the first group of experiments the kidneys in 14 cats were delivered through the usual loin incision with the blood supply and ureter intact. The organ was firmly supported in a cradle and measured blows applied by dropping a known weight on the kidney from predetermined heights, a small vertical rod being used as a guide bar. The resultant trauma was recorded in each instance. It was found that the injury produced varied greatly the size of the kidney probably being a large factor in determining the susceptibility of each organ to such injury. We found that the trauma produced could be conveniently divided into four groups. The first group embraced minor injuries occurring principally in the perirenal fascia and was characterized by petechical hemorrhagic areas about the torn blood vessels with little or no injury to the fibrous capsule or renal 1 Read before the annual meeting of the American Urological Association, Boston, Mass., May 18-21, 1936, and also by invitation before the North Central Branch of the American Urological Association, Cincinnati, Ohio, September 26, 1936.
466
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
467
parenchyma (fig. 1). An interesting finding was the frequent presence of hemorrhagic extravasation from the vessels about the hilum. In seven instances where light blows were applied this was the first injury observed. With blows of slightly greater intensity we frequently found subcapsular extravasation involving the entire surface of the organ. This resulted from the rupture of small blood vessels on the surface of the kidney. We have included in a second group more severe injuries of the kidney characterized by rupture of the fibrous capsule with superficial lacerations of the kidney cortex (fig. 2). Injuries of this type were found in eleven instances. The kidneys were bisected and upon examination showed superficial laceration, except in one instance in which there was a small transverse tear in the medulla about one cm. long, but this did not involve the renal pelvis.
FIG. 1 FIG. 2 FIG. 1. Type I injury. Note presence of small subcapsular hemorrhage but no laceration of cortex. FIG. 2. Type II injury. Laceration of fibrous capsule.
In a third group were included those injuries in which the parenchyma was grossly damaged, varying from moderate to extensive laceration with or without involvement of the renal pelvis (fig. 3). The most striking finding in this connection was that the resistance offered by the kidney to laceration is attributable largely to the protection offered by its perirenal fascia and more especially the fibrous capsule. This is illustrated by the following protocols: Experiment No. 8, a blow of 14.6 kilogram centimeters delivered to the kidney produced no demonstrable injury to the kidney parenchyma and no injury to the perirenal tissues other than small petechial hemorrhagic areas. A blow however of 16. 7 kilogram centimeters, which was found capable of rupturing the capsule, produced extensive laceration of the kidney parenchyma.
468
W. CALHOUN STIRLING AND A. M. LANDS
Experiment No. 9, a blow of 27.1 kilogram centimeters produced a small laceration of the renal capsule just above and over the pelvis in the midportion of the kidney. There was no apparent injury to the parenchyma. The capsule was then stripped off and a second blow of the same intensity applied which crushed the organ almost beyond recognition. Experiment No. 11, a blow of 20.9 kilogram centimeters delivered to the intact kidney caused a tear in the fibrous capsule involving the upper pole. This was very similar to the one previously noted. The kidney was then exci~ed and a careful examination revealed no parenchymal injury. The fibrous capsule was then stripped from the remaining kidney and a blow of the same intensity applied which caused partial pulping of the kidney sub-
FIG. 4 This shows both surface and internal laceration extending into
FIG. 3 FIG.
3. Type III injury.
pelvis. FIG. 4. Type IV injury of kidney with complete separation of organ into three parts, middle one showing pulpifaction.
stance and its separation into three parts. These lacerations extended into the renal pelvis. Experiment No. 11, a blow of 16.7 kilogram centimeters was applied to the intact kidney causing two localized hemorrhages in the perirenal fascia and a rather diffuse subcapsular hemorrhage, but no evidence of rupture of the fibrous capsule or parenchyma. The capsule was then removed from the other kidney and a blow of the same intensity applied. This caused complete laceration of the organ (fig. 4). We believe that these experiments indicate that the resistance offered by the kidney to injury is due, for the most part, to the protection of the perirenal fascia and fibrous capsule. The amount of force necessary to rupture the organ is essentially that which will produce a primary divulsion of the capsule.
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY TABLE
469
1.-Classijication of kidney injuries
EXPERI-
MENT NUMBER
BLO\V
TYPE OF INJURY
Type I kgm. cm.
1R
2L 4R SR
SL 7L
13. 8 8.3 8.3 16. 7 20.9
SR llR
13.8 13.8 20.9
12L
16. 7
Subcapsular ecchymosis Surface contusion Contusion and perivascular extravasation m perirenal tissue. No demonstrable renal damage Definite hemorrhage about hilum Small extravasation in perirenal fascia and a hemorrhagic area. at hilum near the renal vessels Subcapsular hemorrhage and ecchymosis .Multiple punctate hemorrhagic spots in perirenal fascia. \Viele spread subcapsular hemorrhage covering a large portion of the kidney T,vo localized hemorrhages in the perirenal capsule and a rather diffuse subcapsular hemorrhage Type II
lR 2R
30. s 12. 5
3R 4L
8.3 20.9
6L 7R
8 3 13.8
9R 9L llR
20.9 27.1 16. 7 20.9
14L
33.4
lOR
Rupture of the capsule Transverse tearing of fibrous capsule from hilus to edge of kidney. Superficial laceration of parenchyma immediately under the hammer Superficial laceration Detachment of capsule ,vith rupture of a blood vessel in mid-portion just under the hammer. Entire kidney shows marked ecchymosis Cansed several tiny fissure-like lacerations just below the hammer Laceration and stripping of capsule at upper pole from middle third to edge of kidney Rupture of capsule. No laceration of parenchyma observed Rupture of the capsule. Some bleeding from superficial vessels Capsule torn Perivascular and subcapsular bleeding. Tear in the fibrous capsule involving the upper pole. A wedge-shaped tear in the long axis of the kidney Capsule torn Type III
2R
56.2 12.5
SR
25.0
12L
16 7
1R
Some laceration of kidney parenchyma Transverse tearing of fibrous capsule from hilus to edge of kidney. Accompanied by a longitudinal stellate tear of midportion of parenchyma immediately beneath the hammer. Incised kidney shows laceration extending into pelvis Capsule ruptured. Numerous small lacerations of the parenchyma. On incision, some of these were found to extend into pelvis On incision, found a transverse tear between cortex and medulla
THE JOURNAL OF UROLOGY, VOL.
37,
NO, 4
470
W. CALHOUN STIRLING AND A. M. LANDS TABLE
1-Concluded
EXPERI-
MENT
TYPE OF INJURY
BLOW
NUMBER
Type IV kgm. cm.
2L 3L
16. 7 12.3
4L
25.0
SL 6L SL 9L 11L"
25 13.8 14.6 27.0 20.9
12R" 13R 14R
16.7 20.9 16.7
Complete laceration of the kidney with some pulping Mashing under the hammer. Two large lacerations from hilus to outer curvature and completely through the kidney substance Extensive pulpification of kidney in mid-portion both beneath hammer and on opposite side. Found to be ruptured intrarenally and completely On bisection, found two extensive tears extending into pelvis Deeply pulped with 3 large transverse tears almost detaching one pole Extensive laceration Organ was mashed almost beyond recognition Kidney torn into three segments. Lacerations penetrated all the way into the pelvis. Middle portion somewhat pulped Divulsion of the kidney separating into three parts Severely lacerated. Involved every part of kidney Laceration at both poles which extended into pelvis
The fourth group of injuries of the kidney include those cases in which pulpifaction was produced. Separation of one or more poles of the organ is a constant finding (fig. 4). Injuries of this severity were produced in six instances. This point may be illustrated by the following protocol: Experiment No. 13, a blow of 12.5 kilogram centimeters caused no demonstrable injury of the kidney parenchyma. When the force of the blow was increased to 20.9 kilogram centimeters there was extensive laceration of the whole kidney, which on bisection was found to involve every portion of the organ. (See table 1 for complete tabulation of these experiments.) RESPONSE OF THE KIDNEY TO TRAUMA
It has been the experience of many genito-urinary surgeons that the majority of kidney injuries respond to non-operative measures with an apparent functional restoration of the organ. In some instances, however, a preliminary study of the case may reveal little apparent injury to the kidney only later to find the damage to have been more serious necessitating surgical intervention. This fact is brought out in previous publications on this subject by one of us (W. C. S.) where attention was
EXPERIMENTAL STUDY OF INJURIES OE KIDNEY
471
called to the fact that while the majority of such injuries may heal spontaneously, the organ may later become functionless as shown by TABLE EXPERI-
MENT NUMBER
TYPE INJURY
2.-Response of the kidney to trauma
URINALYSIS BLOOD ALBUMIN
DURATION OF EXPERIMENT
REMARKS
- - - ---days
Cats 18 19
I
I
None None
17
II II II
23 27*
II II
28 21*
II III
None None Blood 1 day; albumin 1 day None Blood 3 days; albumin 3 days None None
22*
III
None
25
III
26
III
Blood 2 days; albumin 2 days Blood-albumin
29*
III
33
III
34
III
37
III
20
IV IV
15 16
38
12 13
No evidence capsular autolysis Capsule removed following injury regener-· a ting found at autopsy No evidence gross injury at autopsy Died respiratory infection Laceration healed at autopsy
10 3-died
12 12 9 9-died 5-died 10 2-died 1-died
Blood 1 day; 9 albumin 1 day No blood; albu- 10-died min 10 days Blood 2 days; 11 albumin 6 days 6-died No blood; albumin2 days 2-died Positive Blood and albu- 10--died min 10 days
Dogs 1*
III
Not obtained
14
2* 3*
III III
Not obtained Not obtained
14 12
I
Laceration healed at autopsy Laceration healed. Fat pad ·well organized and firmly attached Cause death? Intact kidney Died respiratory infection reparation well under healed Laceration completely healed only showing thin line of scar Abdominal cavity filled bloody Jluid Large mass of blood about kidney no free blood in abdominal cavity Laceration covered fat pad healing well advanced Necrosis of perirenal tissue extending well into cortex Four extensive lacerations cortex extended into pelvis. Sacrificed Necrosis lower pole site of injury Injury only apparent cause death Necrosis involving cortex and pelvis localized in lower pole Pyelograms made. Kidney healed. eration evidenced by thin scar line Same as Dog 1 Same as Dog 2
Lac-
* Asterisk denotes animals in which surgical repair was done.
subsequent pyelographic studies. In cases of severe laceration with separation of one or more poles or where the renal vessels are torn, nephrectomy was always indicated. (Type IV in our classification.)
472
W. CALHOUN STIRLING AND A. M. LANDS
In order to study the process of repair in the injured kidney, 3 dogs and and 23 cats were subjected to various degrees of injury as previously referred to, and their subsequent reactions followed in the laboratory. (See table 2.) These animals were divided into two groups: (1) Those in which no reparative treatment was given and (b) those in which surgical repair was instituted. A. Kidney injury without repair. In this group the animals were anesthetized with ether and under aseptic conditions the left kidney was delivered. The organ was supported by sterile gauze placed in the costovertebral angle and the desired degree of trauma produced by blows with a broad-faced hammer 4.5 cm. in diameter. This group was composed of two type I, seven type II, five type III, and two type IV injuries. After trauma was applied the kidney was replaced and the incision closed. Urine was collected daily and analyzed for blood and albumin. In two experiments (18 and 19), the usual type I injury characterized by subcapsular hemorrhage was produced. In both instances the animals made uneventful recoveries. In experiment 18, the capsule at autopsy was found to be intact and the parenchyma of a normal color. In experiment 19, following injury, the capsule was carefully dissected from the kidney. When the animal was sacrificed thirteen days later the kidney was found to be covered by a fine film-like tissue representing the regenerating capsule. Neither of these animals showed blood in the urine following the experiment, one however (see table 2) showed albumin for four days. Of the seven type II injuries, hematuria was only found in two instances, the longest duration being three days. In five of the seven experiments classified as type II injuries, the capsule was ruptured by the blows applied. At autopsy the superficial lacerations produced by the trauma were found to be entirely healed and capsular regeneration was well under way. In experiments 28 and 32, the kidneys were traumatized by sharp blows applied with the back of scissors producing extensive subcapsular hemorrhage, but without rupture of the capsule. It is interesting to note that in both instances healing proceeded in a normal manner and at autopsy 11 days later the fibrous capsule was found to be normal. An extensive, well organized blood clot was found beneath the capsule. The kidney was bisected and upon examination the parenchyma injuries were found to be superficial and healed. In five animals receiving type III injuries, the kidneys were left un-
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
473
repaired. Two of these animals (experiments 25 and 26) died within 48 hours, both showing blood in the urine and in one (experiment 25) the abdomen was filled with bloody fluid. A third animal (experiment died on the 8th post-operative day and at autopsy necrosis was found to have occurred in the lower pole of the kidney and in the perirenal tissues near this point. This was the only apparent cause of death. Of the two showed remaining animals (experiments 33 and 34), one (experiment blood in the urine for four days and albumin for six days, the other (experiment 33) showed only albumin which, however, persisted until death which occurred on the 11th post-operative day. In this animal (experiment 33) the kidney was traumatized by repeated blows with the blunt surface of heavy scissors. There was no laceration of the capsule, but there was extensive subcapsular extravasation of blood. When the animal was scari:ficed, the kidney capsule was found to be necrotic, the necrosis extending about mid-way into the cortex. In experiment 34, examination of the kidney at the end of the experiment revealed nothing significantly new. Type IV injuries, characterized by serious laceration and pulpifaction of the kidney, were produced in two animals in this series. One of these died within two days and the other in ten days. In both of these experiments there was much blood in the urine. Lowsley reported his findings following experimental trauma of the dog kidney. The trauma being produced by blows with a blunt dissector. He reports various degrees of parenchymal injury without rupture of the capsule. The difference in his results and those obtained by us is due, in all probability, to the manner in which the trauma was produced. In our experiments the force was applied to a considerable area of the kidney surface thereby producing a marked tension in the fibrous capsule causing its rupture. A blow applied to a relatively small area might produce considerable damage to the kidney parenchyma under the blow without any great increase in capsular tension. This is probably the reason Lowsley observed parenchymal injury without laceration of the fibrous capsule. We believe that the type of blow applied in our experiments is more nearly comparable to those which produce trauma of the kidney in the human. Let us repeat, the resistance offered by the kidney to trauma is largely determined by the strength of its fibrous capsule. It has been reported that the continued hemorrhage and extravasation of urine from the ruptured and macerated
474
W. CALHOUN STIRLING AND A. M. LANDS
cortex results in capsular rupture and abscess formation. In our experiments subcapsular hemorrhage alone in no instance produced autolysis of the fibrous capsule, and further, Tuffier has shown that the exposed surface of the parenchyma does not secrete urine. Extravasation of urine will not occur unless the pelvic cavity has been entered. In one case (experiment 33) autolysis was found and later it was established that there had been laceration extending into the pelvis. Autolysis resulted from the extravasation of urine into the subcapsular space. This fact is borne out by a recent case reported by one of us (W. C. S.) Type I injuries rarely come to the attention of genito-urinary surgeons as there is no hematuria and the only symptoms are local evidences of injury, with pain and tenderness in the kidney region. Conservative treatment is all that is needed in these cases as indicated by both experimental and clinical studies. Injuries belonging to our second type do occasionally come to the attention of the surgeon. There is pain as in type I and hematuria of short duration is not uncommon. With conservative treatment these cases usually will go on to recovery without surgical intervention. The type III injury is characterized clinically by blood in the urine, shock, fall in the blood pressure, the presence of a mass in the loin, lowered red cell count, ileus and positive urographic findings, either excretory or retrograde. When these symptoms are found, the procedure recommended is confinement to bed, a urinalysis, and frequent examination of the blood pressure and x-rayexaminations. Further pyelographic studies during convalescence may be useful. A continuation of the previously mentioned findings or an increase in their severity would indicate conservative operative intervention, i.e., drainage and repairs. We believe that type IV injuries are beyond repair and that nephrectomy is the safest procedure. B. Operative repair of the kidney in experimental animals. As previously brought out, operative treatment is not usually required for types I and IL The kind of operative repair in type III injuries will obviously be determined, in large part, by the nature of the injury. In a group of three dogs and five cats, type III laceration was produced. We would like to emphasize here the value of applying fat to the bleeding surface as a means of checking hemorrhage, as recommended by Koll and by Lowsley. At the termination of the experiments, the transplanted tissue was found to have been incorporated into the kidney substance. Where the laceration was so extensive that the bleed-
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
475
ing could not be arrested by the application of fat alone, the torn surfaces were approximated. To avoid destruction of kidney tissue, the fibrous capsule was utilized as a support whenever possible. Sometimes, especially with the larger kidneys, the organ was held together by ribbon gut as recommended by Lowsley. Even with this type of suture there was some reduction in the size of the organ, but we believe that its use offers many advantages over the older type of sutures used in the repair of kidney injuries. In all of the experiments in which operative repair was resorted to the animals survived the experimental period and when sacrificed, the process of healing was found well advanced (fig. 5).
FIG. 5. Kidney repaired following trauma. healed laceration.
Note the incorporation of fat tissue into
With the kind assistance of Dr. F. 0. Coe, of the Department of Radiology, Georgetown University School of Medicine, we were able to make some excretory pyelograms of dogs following laceration and repair of the kidney. On the basis of these experiments and the study of a large number of clinical cases, we would like to call attention to the following diagnostic points revealed by pyelographic study: 1. The complete absence, in some cases, of a renal shadow on the affected side, but showing a normal pyelogram on the uninjured side (fig. 5). 2. A fan-shaped extravasation of opaque fluid from the minor calyces without alterations in the pelvic outline (fig. 6).
476
W. CALHOUN STIRLING AND A. M. LANDS
FIG. 6. Fan-shaped extravasation of upper pole of right kidney. Capsule not ruptured. Symptomatic treatment effected cure.
Result of direct blow.
FrG. 7. Excretory pyelogram showing variable extention of shadows from right pelvis to capsule. This represents a type III injury (non-operative).
FIG. 8
FIG. 9
FIG. 8. Rupture of left kidney from indirect injury of abdomen.
Lower calyx partially obliterated by blood clot. Subcapsular type injury. Symptomatic treatment effected cure. FIG. 9. Excretory pyelogram showing marked distortion of left pelvic shadow from leakage of pelvis. Type III injury.
FIG. 11 FIG.10 FIG. 10. Retrograde pyelogram showing presence of an extrarenal opaque area. FIG. 11. Complete absence of renal shadow on injured left side. Normal pelvis on opposite side as shown in excretory pyelogram.
477
478
W. CALHOUN STIRLING AND A. M. LANDS
3. A variable extension of shadows from pelvis to capsule (fig. 7). 4. Incomplete and/or irregular filling of the minor calyces as a result of blood clots (fig. 8). 5. Marked distortion of the pelvic shadow from pelvic leakage (fig. 9). 6. Presence of an irregular extrarenal opaque area (fig. 10). 7. Marked displacement of the kidney and distortion of the renal shadow, i.e., transverse or longitudinal compression (fig. 11) . . We should like to express our grateful appreciation to Prof. R. A. Cutting, Department of Physiology, for many helpful suggestions during the course of this investigation, and to Prof. Eugene Whitmore, and the
FIG. 12. Partial atrophy of left kidney; lower calyces almost obliterated. Intravenous pyelogram made eight weeks after expectant treatment. Incision and drainage would have probably restored the function.
Department of Pathology for preparing histological sections. Our thanks are due Mr. W. F. Sheridon for making the photographs. Davis and Geck kindly supplied the ribbon gut used in this study. SUMMARY
On the basis of an experimental study of kidney trauma, we have divided such injuries into four types and described the degree of injury characteristic of each type. Types I and II in our classification are milder injuries and are nonsurgical. Operative repair in type III injuries was successful in all experiments where tried, whereas in 80 per cent of our non-repaired animals the trauma resulted in death.
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
479
N ephrectomy is recommended in type IV injuries. Intravenous pyelography is an important aid both in the diagnosis of kidney trauma and the subsequent functional state of the organ.
1621 Connecticut Ave., N. W., Washington, D. C. REFERENCES KoLL: Transplantation of fat in prostatic and kidney surgery. Jour. Amer. Med. Assoc., 68: 536-538, 1917. KUSTER: Arch. f. Klin. Chir., 1: 671, 1895. LowsLEY: A new method of repairing kidney wounds. Surg., Gynec. and Obstet., 57: 494-500, 1934. LowsLEY: Experimental surgery of the kidney. J our Kans. Med. Soc., October, 1935. STIRLING: Delayed extensive perirenal extravasation of urine following traumatic injury of a kidney. Medical An;nuals, District of Columbia, 3: February, 1934. STIRLING: Traumatism of the kidney. A report of 27 cases. Brit. Jour. Urol., 8: March, 1936. TuFFIER: Etudes Experimentales sur chirurgie du rein, Paris, 1899.
AND
A. M. LANDS
Front the Departments of Urology and Physiology, Georgetown University School of Medicine, Washing/on, D. C.
This experimental study of in juries of the kidney was undertaken: (1) to classify more exactly the type of injury produced, (2) to determine the response of the kidney to injury in both untreated animals and in animals following surgical repair, and (3) to determine the diagnostic value of pyelography in such conditions. Kuster was one of the first investigators to make an experimental study of the factors involved in kidney rupture, his investigations being made on necropsy specimens. The studies here reported were made (with the exception of a few cases) on the intact organ. Tuffier divided injuries of the kidney into three groups, i.e., ecchymosis, subcapsular rupture and total rupture. On the basis of some preliminary studies, we came to the conclusion that this classification was inadequate and that the nature of the reparative response of the kidney to injury should receive further experimental study. Lowsley described the effect on the kidney of instrumental trauma. We have been able to confirm his findings in part and these will be discussed later. This study was undertaken to determine what actually occurred in such injuries. In a series of 40 experimental animals (cats and dogs) we subjected the kidneys to various degrees of trauma. In the first group of experiments the kidneys in 14 cats were delivered through the usual loin incision with the blood supply and ureter intact. The organ was firmly supported in a cradle and measured blows applied by dropping a known weight on the kidney from predetermined heights, a small vertical rod being used as a guide bar. The resultant trauma was recorded in each instance. It was found that the injury produced varied greatly the size of the kidney probably being a large factor in determining the susceptibility of each organ to such injury. We found that the trauma produced could be conveniently divided into four groups. The first group embraced minor injuries occurring principally in the perirenal fascia and was characterized by petechical hemorrhagic areas about the torn blood vessels with little or no injury to the fibrous capsule or renal 1 Read before the annual meeting of the American Urological Association, Boston, Mass., May 18-21, 1936, and also by invitation before the North Central Branch of the American Urological Association, Cincinnati, Ohio, September 26, 1936.
466
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
467
parenchyma (fig. 1). An interesting finding was the frequent presence of hemorrhagic extravasation from the vessels about the hilum. In seven instances where light blows were applied this was the first injury observed. With blows of slightly greater intensity we frequently found subcapsular extravasation involving the entire surface of the organ. This resulted from the rupture of small blood vessels on the surface of the kidney. We have included in a second group more severe injuries of the kidney characterized by rupture of the fibrous capsule with superficial lacerations of the kidney cortex (fig. 2). Injuries of this type were found in eleven instances. The kidneys were bisected and upon examination showed superficial laceration, except in one instance in which there was a small transverse tear in the medulla about one cm. long, but this did not involve the renal pelvis.
FIG. 1 FIG. 2 FIG. 1. Type I injury. Note presence of small subcapsular hemorrhage but no laceration of cortex. FIG. 2. Type II injury. Laceration of fibrous capsule.
In a third group were included those injuries in which the parenchyma was grossly damaged, varying from moderate to extensive laceration with or without involvement of the renal pelvis (fig. 3). The most striking finding in this connection was that the resistance offered by the kidney to laceration is attributable largely to the protection offered by its perirenal fascia and more especially the fibrous capsule. This is illustrated by the following protocols: Experiment No. 8, a blow of 14.6 kilogram centimeters delivered to the kidney produced no demonstrable injury to the kidney parenchyma and no injury to the perirenal tissues other than small petechial hemorrhagic areas. A blow however of 16. 7 kilogram centimeters, which was found capable of rupturing the capsule, produced extensive laceration of the kidney parenchyma.
468
W. CALHOUN STIRLING AND A. M. LANDS
Experiment No. 9, a blow of 27.1 kilogram centimeters produced a small laceration of the renal capsule just above and over the pelvis in the midportion of the kidney. There was no apparent injury to the parenchyma. The capsule was then stripped off and a second blow of the same intensity applied which crushed the organ almost beyond recognition. Experiment No. 11, a blow of 20.9 kilogram centimeters delivered to the intact kidney caused a tear in the fibrous capsule involving the upper pole. This was very similar to the one previously noted. The kidney was then exci~ed and a careful examination revealed no parenchymal injury. The fibrous capsule was then stripped from the remaining kidney and a blow of the same intensity applied which caused partial pulping of the kidney sub-
FIG. 4 This shows both surface and internal laceration extending into
FIG. 3 FIG.
3. Type III injury.
pelvis. FIG. 4. Type IV injury of kidney with complete separation of organ into three parts, middle one showing pulpifaction.
stance and its separation into three parts. These lacerations extended into the renal pelvis. Experiment No. 11, a blow of 16.7 kilogram centimeters was applied to the intact kidney causing two localized hemorrhages in the perirenal fascia and a rather diffuse subcapsular hemorrhage, but no evidence of rupture of the fibrous capsule or parenchyma. The capsule was then removed from the other kidney and a blow of the same intensity applied. This caused complete laceration of the organ (fig. 4). We believe that these experiments indicate that the resistance offered by the kidney to injury is due, for the most part, to the protection of the perirenal fascia and fibrous capsule. The amount of force necessary to rupture the organ is essentially that which will produce a primary divulsion of the capsule.
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY TABLE
469
1.-Classijication of kidney injuries
EXPERI-
MENT NUMBER
BLO\V
TYPE OF INJURY
Type I kgm. cm.
1R
2L 4R SR
SL 7L
13. 8 8.3 8.3 16. 7 20.9
SR llR
13.8 13.8 20.9
12L
16. 7
Subcapsular ecchymosis Surface contusion Contusion and perivascular extravasation m perirenal tissue. No demonstrable renal damage Definite hemorrhage about hilum Small extravasation in perirenal fascia and a hemorrhagic area. at hilum near the renal vessels Subcapsular hemorrhage and ecchymosis .Multiple punctate hemorrhagic spots in perirenal fascia. \Viele spread subcapsular hemorrhage covering a large portion of the kidney T,vo localized hemorrhages in the perirenal capsule and a rather diffuse subcapsular hemorrhage Type II
lR 2R
30. s 12. 5
3R 4L
8.3 20.9
6L 7R
8 3 13.8
9R 9L llR
20.9 27.1 16. 7 20.9
14L
33.4
lOR
Rupture of the capsule Transverse tearing of fibrous capsule from hilus to edge of kidney. Superficial laceration of parenchyma immediately under the hammer Superficial laceration Detachment of capsule ,vith rupture of a blood vessel in mid-portion just under the hammer. Entire kidney shows marked ecchymosis Cansed several tiny fissure-like lacerations just below the hammer Laceration and stripping of capsule at upper pole from middle third to edge of kidney Rupture of capsule. No laceration of parenchyma observed Rupture of the capsule. Some bleeding from superficial vessels Capsule torn Perivascular and subcapsular bleeding. Tear in the fibrous capsule involving the upper pole. A wedge-shaped tear in the long axis of the kidney Capsule torn Type III
2R
56.2 12.5
SR
25.0
12L
16 7
1R
Some laceration of kidney parenchyma Transverse tearing of fibrous capsule from hilus to edge of kidney. Accompanied by a longitudinal stellate tear of midportion of parenchyma immediately beneath the hammer. Incised kidney shows laceration extending into pelvis Capsule ruptured. Numerous small lacerations of the parenchyma. On incision, some of these were found to extend into pelvis On incision, found a transverse tear between cortex and medulla
THE JOURNAL OF UROLOGY, VOL.
37,
NO, 4
470
W. CALHOUN STIRLING AND A. M. LANDS TABLE
1-Concluded
EXPERI-
MENT
TYPE OF INJURY
BLOW
NUMBER
Type IV kgm. cm.
2L 3L
16. 7 12.3
4L
25.0
SL 6L SL 9L 11L"
25 13.8 14.6 27.0 20.9
12R" 13R 14R
16.7 20.9 16.7
Complete laceration of the kidney with some pulping Mashing under the hammer. Two large lacerations from hilus to outer curvature and completely through the kidney substance Extensive pulpification of kidney in mid-portion both beneath hammer and on opposite side. Found to be ruptured intrarenally and completely On bisection, found two extensive tears extending into pelvis Deeply pulped with 3 large transverse tears almost detaching one pole Extensive laceration Organ was mashed almost beyond recognition Kidney torn into three segments. Lacerations penetrated all the way into the pelvis. Middle portion somewhat pulped Divulsion of the kidney separating into three parts Severely lacerated. Involved every part of kidney Laceration at both poles which extended into pelvis
The fourth group of injuries of the kidney include those cases in which pulpifaction was produced. Separation of one or more poles of the organ is a constant finding (fig. 4). Injuries of this severity were produced in six instances. This point may be illustrated by the following protocol: Experiment No. 13, a blow of 12.5 kilogram centimeters caused no demonstrable injury of the kidney parenchyma. When the force of the blow was increased to 20.9 kilogram centimeters there was extensive laceration of the whole kidney, which on bisection was found to involve every portion of the organ. (See table 1 for complete tabulation of these experiments.) RESPONSE OF THE KIDNEY TO TRAUMA
It has been the experience of many genito-urinary surgeons that the majority of kidney injuries respond to non-operative measures with an apparent functional restoration of the organ. In some instances, however, a preliminary study of the case may reveal little apparent injury to the kidney only later to find the damage to have been more serious necessitating surgical intervention. This fact is brought out in previous publications on this subject by one of us (W. C. S.) where attention was
EXPERIMENTAL STUDY OF INJURIES OE KIDNEY
471
called to the fact that while the majority of such injuries may heal spontaneously, the organ may later become functionless as shown by TABLE EXPERI-
MENT NUMBER
TYPE INJURY
2.-Response of the kidney to trauma
URINALYSIS BLOOD ALBUMIN
DURATION OF EXPERIMENT
REMARKS
- - - ---days
Cats 18 19
I
I
None None
17
II II II
23 27*
II II
28 21*
II III
None None Blood 1 day; albumin 1 day None Blood 3 days; albumin 3 days None None
22*
III
None
25
III
26
III
Blood 2 days; albumin 2 days Blood-albumin
29*
III
33
III
34
III
37
III
20
IV IV
15 16
38
12 13
No evidence capsular autolysis Capsule removed following injury regener-· a ting found at autopsy No evidence gross injury at autopsy Died respiratory infection Laceration healed at autopsy
10 3-died
12 12 9 9-died 5-died 10 2-died 1-died
Blood 1 day; 9 albumin 1 day No blood; albu- 10-died min 10 days Blood 2 days; 11 albumin 6 days 6-died No blood; albumin2 days 2-died Positive Blood and albu- 10--died min 10 days
Dogs 1*
III
Not obtained
14
2* 3*
III III
Not obtained Not obtained
14 12
I
Laceration healed at autopsy Laceration healed. Fat pad ·well organized and firmly attached Cause death? Intact kidney Died respiratory infection reparation well under healed Laceration completely healed only showing thin line of scar Abdominal cavity filled bloody Jluid Large mass of blood about kidney no free blood in abdominal cavity Laceration covered fat pad healing well advanced Necrosis of perirenal tissue extending well into cortex Four extensive lacerations cortex extended into pelvis. Sacrificed Necrosis lower pole site of injury Injury only apparent cause death Necrosis involving cortex and pelvis localized in lower pole Pyelograms made. Kidney healed. eration evidenced by thin scar line Same as Dog 1 Same as Dog 2
Lac-
* Asterisk denotes animals in which surgical repair was done.
subsequent pyelographic studies. In cases of severe laceration with separation of one or more poles or where the renal vessels are torn, nephrectomy was always indicated. (Type IV in our classification.)
472
W. CALHOUN STIRLING AND A. M. LANDS
In order to study the process of repair in the injured kidney, 3 dogs and and 23 cats were subjected to various degrees of injury as previously referred to, and their subsequent reactions followed in the laboratory. (See table 2.) These animals were divided into two groups: (1) Those in which no reparative treatment was given and (b) those in which surgical repair was instituted. A. Kidney injury without repair. In this group the animals were anesthetized with ether and under aseptic conditions the left kidney was delivered. The organ was supported by sterile gauze placed in the costovertebral angle and the desired degree of trauma produced by blows with a broad-faced hammer 4.5 cm. in diameter. This group was composed of two type I, seven type II, five type III, and two type IV injuries. After trauma was applied the kidney was replaced and the incision closed. Urine was collected daily and analyzed for blood and albumin. In two experiments (18 and 19), the usual type I injury characterized by subcapsular hemorrhage was produced. In both instances the animals made uneventful recoveries. In experiment 18, the capsule at autopsy was found to be intact and the parenchyma of a normal color. In experiment 19, following injury, the capsule was carefully dissected from the kidney. When the animal was sacrificed thirteen days later the kidney was found to be covered by a fine film-like tissue representing the regenerating capsule. Neither of these animals showed blood in the urine following the experiment, one however (see table 2) showed albumin for four days. Of the seven type II injuries, hematuria was only found in two instances, the longest duration being three days. In five of the seven experiments classified as type II injuries, the capsule was ruptured by the blows applied. At autopsy the superficial lacerations produced by the trauma were found to be entirely healed and capsular regeneration was well under way. In experiments 28 and 32, the kidneys were traumatized by sharp blows applied with the back of scissors producing extensive subcapsular hemorrhage, but without rupture of the capsule. It is interesting to note that in both instances healing proceeded in a normal manner and at autopsy 11 days later the fibrous capsule was found to be normal. An extensive, well organized blood clot was found beneath the capsule. The kidney was bisected and upon examination the parenchyma injuries were found to be superficial and healed. In five animals receiving type III injuries, the kidneys were left un-
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
473
repaired. Two of these animals (experiments 25 and 26) died within 48 hours, both showing blood in the urine and in one (experiment 25) the abdomen was filled with bloody fluid. A third animal (experiment died on the 8th post-operative day and at autopsy necrosis was found to have occurred in the lower pole of the kidney and in the perirenal tissues near this point. This was the only apparent cause of death. Of the two showed remaining animals (experiments 33 and 34), one (experiment blood in the urine for four days and albumin for six days, the other (experiment 33) showed only albumin which, however, persisted until death which occurred on the 11th post-operative day. In this animal (experiment 33) the kidney was traumatized by repeated blows with the blunt surface of heavy scissors. There was no laceration of the capsule, but there was extensive subcapsular extravasation of blood. When the animal was scari:ficed, the kidney capsule was found to be necrotic, the necrosis extending about mid-way into the cortex. In experiment 34, examination of the kidney at the end of the experiment revealed nothing significantly new. Type IV injuries, characterized by serious laceration and pulpifaction of the kidney, were produced in two animals in this series. One of these died within two days and the other in ten days. In both of these experiments there was much blood in the urine. Lowsley reported his findings following experimental trauma of the dog kidney. The trauma being produced by blows with a blunt dissector. He reports various degrees of parenchymal injury without rupture of the capsule. The difference in his results and those obtained by us is due, in all probability, to the manner in which the trauma was produced. In our experiments the force was applied to a considerable area of the kidney surface thereby producing a marked tension in the fibrous capsule causing its rupture. A blow applied to a relatively small area might produce considerable damage to the kidney parenchyma under the blow without any great increase in capsular tension. This is probably the reason Lowsley observed parenchymal injury without laceration of the fibrous capsule. We believe that the type of blow applied in our experiments is more nearly comparable to those which produce trauma of the kidney in the human. Let us repeat, the resistance offered by the kidney to trauma is largely determined by the strength of its fibrous capsule. It has been reported that the continued hemorrhage and extravasation of urine from the ruptured and macerated
474
W. CALHOUN STIRLING AND A. M. LANDS
cortex results in capsular rupture and abscess formation. In our experiments subcapsular hemorrhage alone in no instance produced autolysis of the fibrous capsule, and further, Tuffier has shown that the exposed surface of the parenchyma does not secrete urine. Extravasation of urine will not occur unless the pelvic cavity has been entered. In one case (experiment 33) autolysis was found and later it was established that there had been laceration extending into the pelvis. Autolysis resulted from the extravasation of urine into the subcapsular space. This fact is borne out by a recent case reported by one of us (W. C. S.) Type I injuries rarely come to the attention of genito-urinary surgeons as there is no hematuria and the only symptoms are local evidences of injury, with pain and tenderness in the kidney region. Conservative treatment is all that is needed in these cases as indicated by both experimental and clinical studies. Injuries belonging to our second type do occasionally come to the attention of the surgeon. There is pain as in type I and hematuria of short duration is not uncommon. With conservative treatment these cases usually will go on to recovery without surgical intervention. The type III injury is characterized clinically by blood in the urine, shock, fall in the blood pressure, the presence of a mass in the loin, lowered red cell count, ileus and positive urographic findings, either excretory or retrograde. When these symptoms are found, the procedure recommended is confinement to bed, a urinalysis, and frequent examination of the blood pressure and x-rayexaminations. Further pyelographic studies during convalescence may be useful. A continuation of the previously mentioned findings or an increase in their severity would indicate conservative operative intervention, i.e., drainage and repairs. We believe that type IV injuries are beyond repair and that nephrectomy is the safest procedure. B. Operative repair of the kidney in experimental animals. As previously brought out, operative treatment is not usually required for types I and IL The kind of operative repair in type III injuries will obviously be determined, in large part, by the nature of the injury. In a group of three dogs and five cats, type III laceration was produced. We would like to emphasize here the value of applying fat to the bleeding surface as a means of checking hemorrhage, as recommended by Koll and by Lowsley. At the termination of the experiments, the transplanted tissue was found to have been incorporated into the kidney substance. Where the laceration was so extensive that the bleed-
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
475
ing could not be arrested by the application of fat alone, the torn surfaces were approximated. To avoid destruction of kidney tissue, the fibrous capsule was utilized as a support whenever possible. Sometimes, especially with the larger kidneys, the organ was held together by ribbon gut as recommended by Lowsley. Even with this type of suture there was some reduction in the size of the organ, but we believe that its use offers many advantages over the older type of sutures used in the repair of kidney injuries. In all of the experiments in which operative repair was resorted to the animals survived the experimental period and when sacrificed, the process of healing was found well advanced (fig. 5).
FIG. 5. Kidney repaired following trauma. healed laceration.
Note the incorporation of fat tissue into
With the kind assistance of Dr. F. 0. Coe, of the Department of Radiology, Georgetown University School of Medicine, we were able to make some excretory pyelograms of dogs following laceration and repair of the kidney. On the basis of these experiments and the study of a large number of clinical cases, we would like to call attention to the following diagnostic points revealed by pyelographic study: 1. The complete absence, in some cases, of a renal shadow on the affected side, but showing a normal pyelogram on the uninjured side (fig. 5). 2. A fan-shaped extravasation of opaque fluid from the minor calyces without alterations in the pelvic outline (fig. 6).
476
W. CALHOUN STIRLING AND A. M. LANDS
FIG. 6. Fan-shaped extravasation of upper pole of right kidney. Capsule not ruptured. Symptomatic treatment effected cure.
Result of direct blow.
FrG. 7. Excretory pyelogram showing variable extention of shadows from right pelvis to capsule. This represents a type III injury (non-operative).
FIG. 8
FIG. 9
FIG. 8. Rupture of left kidney from indirect injury of abdomen.
Lower calyx partially obliterated by blood clot. Subcapsular type injury. Symptomatic treatment effected cure. FIG. 9. Excretory pyelogram showing marked distortion of left pelvic shadow from leakage of pelvis. Type III injury.
FIG. 11 FIG.10 FIG. 10. Retrograde pyelogram showing presence of an extrarenal opaque area. FIG. 11. Complete absence of renal shadow on injured left side. Normal pelvis on opposite side as shown in excretory pyelogram.
477
478
W. CALHOUN STIRLING AND A. M. LANDS
3. A variable extension of shadows from pelvis to capsule (fig. 7). 4. Incomplete and/or irregular filling of the minor calyces as a result of blood clots (fig. 8). 5. Marked distortion of the pelvic shadow from pelvic leakage (fig. 9). 6. Presence of an irregular extrarenal opaque area (fig. 10). 7. Marked displacement of the kidney and distortion of the renal shadow, i.e., transverse or longitudinal compression (fig. 11) . . We should like to express our grateful appreciation to Prof. R. A. Cutting, Department of Physiology, for many helpful suggestions during the course of this investigation, and to Prof. Eugene Whitmore, and the
FIG. 12. Partial atrophy of left kidney; lower calyces almost obliterated. Intravenous pyelogram made eight weeks after expectant treatment. Incision and drainage would have probably restored the function.
Department of Pathology for preparing histological sections. Our thanks are due Mr. W. F. Sheridon for making the photographs. Davis and Geck kindly supplied the ribbon gut used in this study. SUMMARY
On the basis of an experimental study of kidney trauma, we have divided such injuries into four types and described the degree of injury characteristic of each type. Types I and II in our classification are milder injuries and are nonsurgical. Operative repair in type III injuries was successful in all experiments where tried, whereas in 80 per cent of our non-repaired animals the trauma resulted in death.
EXPERIMENTAL STUDY OF INJURIES OF KIDNEY
479
N ephrectomy is recommended in type IV injuries. Intravenous pyelography is an important aid both in the diagnosis of kidney trauma and the subsequent functional state of the organ.
1621 Connecticut Ave., N. W., Washington, D. C. REFERENCES KoLL: Transplantation of fat in prostatic and kidney surgery. Jour. Amer. Med. Assoc., 68: 536-538, 1917. KUSTER: Arch. f. Klin. Chir., 1: 671, 1895. LowsLEY: A new method of repairing kidney wounds. Surg., Gynec. and Obstet., 57: 494-500, 1934. LowsLEY: Experimental surgery of the kidney. J our Kans. Med. Soc., October, 1935. STIRLING: Delayed extensive perirenal extravasation of urine following traumatic injury of a kidney. Medical An;nuals, District of Columbia, 3: February, 1934. STIRLING: Traumatism of the kidney. A report of 27 cases. Brit. Jour. Urol., 8: March, 1936. TuFFIER: Etudes Experimentales sur chirurgie du rein, Paris, 1899.