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Indications for Surgery in Diverticulitis
Indications for Surgery in Diverticulitis BENTLEY P. COLCOCK, M.D.
For many years the indications for surgery in diverticulitis have been limited to the complications of this disease. When a perforation, complete obstruction, or fistula develops in a patient with diverticulitis, it is obvious that the patient must be operated on, and, in most instances, operated on promptly. Indeed, the patient's life may depend on how quickly and how well that operation is carried out. Surgeons know that a direct attack upon the inflammatory mass is dangerous. Complications, such as residual abscesEes, are common and sometimes lead to the patient's death. Before the staged operative approach was adopted, the mortality rate for the surgical treatment of diverticulitis was 40 per cent. If, however, the primary lesion is not disturbed, but simply excluded by a proximal colostomy, the inflammatory reaction will subside. This was found to be true even without the help of the antibiotics. If the abscess is large, resolution can be hastened by incision and drainage, but the essential point in the surgical management is diversion of the fecal stream. The same is true for the patient with complete obstruction or a colovesical fistula. Later the involved segment of colon is removed and the colostomy closed. This staged method of attack has brought the mortality rate, even for those patients with the complications of diverticulitis, to less than 5 per cent. Despite this tremendous improvement, many surgeons interested in diverticulitis are disturbed by the persistent high morbidity rate. Emergency surgery on an acutely ill patient, followed by resection of the large intestine, and closure of the colostomy, adds up to many weeks in the hospital. If the patient is not willing to return to work with his colostomy he may be out of work for six to nine months. Occasionally, the colostomy can be closed at the time of the resection, which will reduce the number of operative procedures to two. But this merely eliminates the least of the operations. If there should be a leak at the suture line, the morbidity will be increased rather than decreased. The morbidity can be significantly reduced only by the increased use of a one-stage resection. The only way that this can be done safely is by operating on these patients before perforation or obstruction occurs or a fistula develops. Experience has shown 785
786
BENTLEY
P.
COLCOCK
that, at this stage, the inflammatory lesion in the sigmoid can be removed and a primary anastomosis carried out with a very low mortality rate. It remains only to select those patients with diverticulitis in whom one of these serious complications is likely to develop and to operate on them before this occurs. In most instances this can be done, and today persistent or recurrent diverticulitis has become the most frequent indication for surgery in this disease. Another indication for surgery in these patients should never be forgotten. Cancer of the colon must be definitely ruled out in every patient with diverticulitis. The sigmoid colon is the most common site for cancer in the entire intestinal tract except for the rectum. Also, 98 per cent of all diverticulitis occurs at this site. Inevitably, both conditions will be present in some patients. Thus, the differential diagnosis may be difficult. The age and sex incidence in both diseases are the same. All too often the symptoms of both diverticulitis and cancer are identical-distress in the left lower quadrant, change in bowel habit, and some rectal bleeding. Tragedies have occurred when patients with carcinoma of the sigmoid colon have been treated for months for diverticulitis. Unless cancer has definitely been ruled out, the patient with "diverticulitis" must be operated on. SPECIFIC INDICATIONS
Perforation Perforation is the most serious of all of the complications of diverticulitis. It can result in spreading or generalized peritonitis within a few hours. A transverse colostomy should be established immediately. This is followed by treatment for the peritonitis-antibiotics, intestinal intubation, replacement of fluids and electrolytes, and so forth. It may be obvious when the patient is first seen that the perforation has been contained and a localized abscess is present. He should be hospitalized and a proximal colostomy performed as an elective procedure. If the mass is very large, excision and drainage by an extraperitoneal approach will hasten its resolution, although this is not absolutely necessary. The proximal portion of the transverse colon is used to form the colostomy (Fig. 1, a). It allows easy mobilization of the splenic flexure and distal transverse colon at the time of the subsequent resection. This will be necessary if the sigmoid colon is not redundant, or if the inflammatory process involves the descending colon. I like to free the splenic flexure if the descending colon has many diverticula. If an anastomosis is made in a segment of the colon containing many diverticula, some of the sutures are bound to pass through these thin-walled sacs. This may result in a leak. The time interval between the colostomy and resection of the bowel (Fig. 1, b) is governed by two factors. The first and most urgent is the need to rule out cancer. Here, the history may be helpful. Symptoms for
INDICATIONS FOR SURGERY IN DIVERTICULITIS
787
Figure 1. a, A Mikulicz spur is not necessary, but the bowel should be completely divided. b, If the involved area is low and the sigmoid is redundant, it may not be necessary to drop the splenic flexure. c, The colostomy is closed by an end-to-end anastomosis.
over a year-marked left lower quadrant pain, tenderness, little or no rectal bleeding-point to diverticulitis rather than cancer. The physician must keep in mind, however, that the patient may have both lesions. Unfortunately, the proctoscopic examination rarely excludes cancer because the edema of the mucosa prevents visualization of the involved area. We are forced to rely, to a large extent, upon the barium enema examination. In our experience, x-ray examination after a barium enema will exclude cancer in only 70 per cent of patients. In 20 per cent the roentgenologist cannot be sure, and in 10 per cent the obstruction is so marked that the barium does not outline the lesion. If repeat studies and the clinical picture fail to exclude cancer, the surgeon is forced to proceed with resection in two to four weeks. The inflammatory reaction is still present and the surgical risk is definitely increased, but this is the lesser of two evils if cancer may be present. If cancer can be ruled out, the resection should not be performed for at least four months. Six months is preferable if a large abscess has been present or a large inflammatory mass surrounds a fistula. At the end of this time the inflammation will usually have subsided, the operation can be carried out in a clean field, and the anastomosis made with normal bowel. Postoperative complications are few. If this interval is shortened, the surgeon runs the risk of losing the great advantage of the staged operative attack. I have frequently closed the colostomy at the time of the resection. This should not be done, however, unless the integrity of the anastomosis is assured. A small defect at the suture line, in the presence of a proximal colostomy, will do no harm. With the proximal colostomy closed, it will lead to an abscess or fistula.
788
BENTLEY
P.
COLCOCK
The colostomy can be safely closed two to four weeks after the resection. The divided bowel is joined by an end-to-end anastomosis and replaced in the peritoneal cavity (Fig. 1, c).
Obstruction With repeated attacks of diverticulitis the intestinal wall becomes thicker and the lumen becomes smaller. The edema associated with another attack may then cause complete obstruction of the colon. This is a serious situation. Unless the obstruction is relieved, distention of the large bowel develops, and secondary perforation (usually in the cecum) may occur. The situation is complicated by the fact that we do not know how close to perforation the inflamed diverticulum may be. Thus, any attempt to relieve the obstruction by enemas is hazardous. Decompression from above by a Miller-Abbott or Cantor tube will merely relieve the small bowel distention. If the proximal colon remains greatly dilated, the safest course is to perform a transverse colostomy. When the inflammatory process is less extensive, the time interval between the colostomy and the resection may be shortened. This observer is impressed, however, with the length of time necessary for diverticulitis to subside. If the surgeon decides to perform the resection less than four months after the colostomy, he may find that he is working in an infected field, with indurated inflamed bowel. This means that he has lost the main value of the staged operative approach.
Fistula A fistula may be external or internal. The most common internal fistula is a colovesical fistula in the male. In a man with diverticulitis the colon usually becomes adherent to the bladder. If the inflammation continues it can lead to a colovesical fistula. For this reason, dysuria is an ominous sign in a man with diverticulitis. Sometimes the patient does not become alarmed until he begins to pass gas from his penis. When this occurs a fistula is already present. In a woman, a fistula is more likely to develop between the colon and vagina. This is particularly true if a hysterectomy has been performed. In some instances a one-stage resection with primary anastomosis can safely be performed when a complication of diverticulitis is present, such as a small and well localized perforation. With care and a good suction apparatus, contamination of the peritoneal cavity is unlikely. A one-stage resection can be done if an obstruction is only partial and the colon is not greatly distended. A one-stage resection can also be carried out if the inflammatory reaction surrounding a fistula is not extensive. It should never be done, however, without a careful evaluation of the risks involved. We should never forget that, when properly carried out, the multiple-stage approach is associated with almost no mortality and very few complications.
INDICATIONS FOR SURGERY IN DIVERTICULITIS
789
Hemorrhage In our experience, severe, persistent bleeding is a rare indication for surgery in patients with diverticulitis. Profuse bleeding is not common and when it does occur it will usually respond to conservative treatment. It may occur in patients who have diverticulosis with little or no diverticulitis. In none of the 150 patients operated on between 1950 and 1960 was bleeding the reason for surgical intervention. Many of these patients had had gross rectal bleeding but even in these patients, another cause for the bleeding-adenomatous polyps or large internal hemorrhoids-was often present. Indeed, a history of rectal bleeding in a patient with a localized lesion of the sigmoid colon should make the surgeon think first of cancer. *
Exclusion of Cancer A careful review of the history, the physical findings, and the barium enema study will rule out cancer in most patients. In a few patients, however, the duration of symptoms will be brief, the febrile reaction will be minimal and rectal bleeding may be frequent. If the barium enema study is equivocal, these patients must be operated on without further delay. Even with the abdomen open the surgeon may not be able to exclude cancer. He must then resect the bowel and its mesentery as he would for carcinoma. This will make the operative procedure more difficult and the likelihood of postoperative complications greater, but the surgeon has no choice. To treat such a patient for months, or to do a limited segmental resection in the belief that the lesion is just diverticulitis, may cost the patient his life.
Recurrent or Persistent Diverticulitis The time has come for surgeons to accept the challenge of reducing the morbidity as well as the mortality of the surgical treatment of diverticulitis. This can be done in two ways. First, operative procedures which are unsatisfactory for the treatment of this disease should be eliminated. Incision and drainage of an abscess resulting from a perforation usually produces a fecal fistula. The same is true for excision of a diverticulum or suture of a fistulous opening. Closure of the colostomy without resection of the diseased bowel usually ends in a recurrence of symptoms and often of the complication. We have seen patients who have had seven or eight operative procedures on their colon, but the complication of diverticulitis that they started with was still present. It is obvious, however, that even when the procedure is applied correctly, the morbidity of the surgical treatment of complicated diverticulitis is high. It will remain high as long as the surgical approach is delayed until perforation or obstruction occurs or a fistula develops. The finding of
* Colcock, B. P. and Sass, R. E.: Diverticulitis and carcinoma of the colon; differential diagnosis. Surg. Gynec. and Obst. 99: 627-633 (Nov.) 1954.
790
BENTLEY
P.
COLCOCK
diverticulosis without symptoms is not an indication for surgery. Mild discomfort in the left lower quadrant when diverticulosis is present may be entirely the result of an irritable colon. When the pain is recurrent and is associated with some fever, it probably indicates the development of diverticulitis. The same is true for the patient with left lower quadrant pain and a palpable mass. When these symptoms persist or increase in severity, elective resection of the diseased bowel should be seriously considered. In patients who have a significantly narrowed sigmoid on barium enema examination, complete obstruction may develop with their next attack. Dysuria in a patient with diverticulitis often precedes a colovesical fistula. I feel that any patient who has had two or more acute attacks (severe enough to suggest a small perforation) should have an operation. These patients are three times as likely to have a serious complication as is the patient who has had but one attack of diverticulitis. All of these complications are more frequent in patients who are under 55 years of age. Thus, to a large extent, we can recognize those patients with diverticulitis who are likely to have a complication of the disease. If they are operated on when the inflammatory reaction is well localized and the bowel is not distended, the morbidity of this disease can be greatly reduced. They require but one operation, and spend less than two weeks in the hospital. They require a minimum of medical and nursing care and are rarely out of work for more than six weeks. They are permanently relieved of their symptoms and they avoid the dangers of a serious complication. Most important of all, this can be done with a very low operative risk. No deaths occurred in this group of 150 patients operated on for diverticulitis between 1950 and 1960 even though 70 per cent had but one operation. It is only when the surgeon attempts the one-stage resection in patients with an extensive inflammatory process, or with a greatly distended bowel, that he is likely to run into difficulty.
SUMMARY
Diverticulitis may lead to three serious complications: perforation of the colon, obstruction of the colon, or a fecal fistula. When this happens, the first responsibility of the surgeon is to save that patient's life. This can be done by a well-planned, multiple-stage, operative procedure. Such a patient will survive, but he will also spend many weeks in the hospital. Two, and possibly three operations will be required and the patient must have a colostomy for several months. This can be avoided by operating on patients with persistent or recurrent diverticulitis before these complications develop. They can then be permanently relieved of their symptoms by one operation and will spend less than two weeks in the hospital. Also, the tragic result of allowing a carcinoma of the colon to go untreated is avoided. The operative risk at this stage is less than 1 per cent.
For many years the indications for surgery in diverticulitis have been limited to the complications of this disease. When a perforation, complete obstruction, or fistula develops in a patient with diverticulitis, it is obvious that the patient must be operated on, and, in most instances, operated on promptly. Indeed, the patient's life may depend on how quickly and how well that operation is carried out. Surgeons know that a direct attack upon the inflammatory mass is dangerous. Complications, such as residual abscesEes, are common and sometimes lead to the patient's death. Before the staged operative approach was adopted, the mortality rate for the surgical treatment of diverticulitis was 40 per cent. If, however, the primary lesion is not disturbed, but simply excluded by a proximal colostomy, the inflammatory reaction will subside. This was found to be true even without the help of the antibiotics. If the abscess is large, resolution can be hastened by incision and drainage, but the essential point in the surgical management is diversion of the fecal stream. The same is true for the patient with complete obstruction or a colovesical fistula. Later the involved segment of colon is removed and the colostomy closed. This staged method of attack has brought the mortality rate, even for those patients with the complications of diverticulitis, to less than 5 per cent. Despite this tremendous improvement, many surgeons interested in diverticulitis are disturbed by the persistent high morbidity rate. Emergency surgery on an acutely ill patient, followed by resection of the large intestine, and closure of the colostomy, adds up to many weeks in the hospital. If the patient is not willing to return to work with his colostomy he may be out of work for six to nine months. Occasionally, the colostomy can be closed at the time of the resection, which will reduce the number of operative procedures to two. But this merely eliminates the least of the operations. If there should be a leak at the suture line, the morbidity will be increased rather than decreased. The morbidity can be significantly reduced only by the increased use of a one-stage resection. The only way that this can be done safely is by operating on these patients before perforation or obstruction occurs or a fistula develops. Experience has shown 785
786
BENTLEY
P.
COLCOCK
that, at this stage, the inflammatory lesion in the sigmoid can be removed and a primary anastomosis carried out with a very low mortality rate. It remains only to select those patients with diverticulitis in whom one of these serious complications is likely to develop and to operate on them before this occurs. In most instances this can be done, and today persistent or recurrent diverticulitis has become the most frequent indication for surgery in this disease. Another indication for surgery in these patients should never be forgotten. Cancer of the colon must be definitely ruled out in every patient with diverticulitis. The sigmoid colon is the most common site for cancer in the entire intestinal tract except for the rectum. Also, 98 per cent of all diverticulitis occurs at this site. Inevitably, both conditions will be present in some patients. Thus, the differential diagnosis may be difficult. The age and sex incidence in both diseases are the same. All too often the symptoms of both diverticulitis and cancer are identical-distress in the left lower quadrant, change in bowel habit, and some rectal bleeding. Tragedies have occurred when patients with carcinoma of the sigmoid colon have been treated for months for diverticulitis. Unless cancer has definitely been ruled out, the patient with "diverticulitis" must be operated on. SPECIFIC INDICATIONS
Perforation Perforation is the most serious of all of the complications of diverticulitis. It can result in spreading or generalized peritonitis within a few hours. A transverse colostomy should be established immediately. This is followed by treatment for the peritonitis-antibiotics, intestinal intubation, replacement of fluids and electrolytes, and so forth. It may be obvious when the patient is first seen that the perforation has been contained and a localized abscess is present. He should be hospitalized and a proximal colostomy performed as an elective procedure. If the mass is very large, excision and drainage by an extraperitoneal approach will hasten its resolution, although this is not absolutely necessary. The proximal portion of the transverse colon is used to form the colostomy (Fig. 1, a). It allows easy mobilization of the splenic flexure and distal transverse colon at the time of the subsequent resection. This will be necessary if the sigmoid colon is not redundant, or if the inflammatory process involves the descending colon. I like to free the splenic flexure if the descending colon has many diverticula. If an anastomosis is made in a segment of the colon containing many diverticula, some of the sutures are bound to pass through these thin-walled sacs. This may result in a leak. The time interval between the colostomy and resection of the bowel (Fig. 1, b) is governed by two factors. The first and most urgent is the need to rule out cancer. Here, the history may be helpful. Symptoms for
INDICATIONS FOR SURGERY IN DIVERTICULITIS
787
Figure 1. a, A Mikulicz spur is not necessary, but the bowel should be completely divided. b, If the involved area is low and the sigmoid is redundant, it may not be necessary to drop the splenic flexure. c, The colostomy is closed by an end-to-end anastomosis.
over a year-marked left lower quadrant pain, tenderness, little or no rectal bleeding-point to diverticulitis rather than cancer. The physician must keep in mind, however, that the patient may have both lesions. Unfortunately, the proctoscopic examination rarely excludes cancer because the edema of the mucosa prevents visualization of the involved area. We are forced to rely, to a large extent, upon the barium enema examination. In our experience, x-ray examination after a barium enema will exclude cancer in only 70 per cent of patients. In 20 per cent the roentgenologist cannot be sure, and in 10 per cent the obstruction is so marked that the barium does not outline the lesion. If repeat studies and the clinical picture fail to exclude cancer, the surgeon is forced to proceed with resection in two to four weeks. The inflammatory reaction is still present and the surgical risk is definitely increased, but this is the lesser of two evils if cancer may be present. If cancer can be ruled out, the resection should not be performed for at least four months. Six months is preferable if a large abscess has been present or a large inflammatory mass surrounds a fistula. At the end of this time the inflammation will usually have subsided, the operation can be carried out in a clean field, and the anastomosis made with normal bowel. Postoperative complications are few. If this interval is shortened, the surgeon runs the risk of losing the great advantage of the staged operative attack. I have frequently closed the colostomy at the time of the resection. This should not be done, however, unless the integrity of the anastomosis is assured. A small defect at the suture line, in the presence of a proximal colostomy, will do no harm. With the proximal colostomy closed, it will lead to an abscess or fistula.
788
BENTLEY
P.
COLCOCK
The colostomy can be safely closed two to four weeks after the resection. The divided bowel is joined by an end-to-end anastomosis and replaced in the peritoneal cavity (Fig. 1, c).
Obstruction With repeated attacks of diverticulitis the intestinal wall becomes thicker and the lumen becomes smaller. The edema associated with another attack may then cause complete obstruction of the colon. This is a serious situation. Unless the obstruction is relieved, distention of the large bowel develops, and secondary perforation (usually in the cecum) may occur. The situation is complicated by the fact that we do not know how close to perforation the inflamed diverticulum may be. Thus, any attempt to relieve the obstruction by enemas is hazardous. Decompression from above by a Miller-Abbott or Cantor tube will merely relieve the small bowel distention. If the proximal colon remains greatly dilated, the safest course is to perform a transverse colostomy. When the inflammatory process is less extensive, the time interval between the colostomy and the resection may be shortened. This observer is impressed, however, with the length of time necessary for diverticulitis to subside. If the surgeon decides to perform the resection less than four months after the colostomy, he may find that he is working in an infected field, with indurated inflamed bowel. This means that he has lost the main value of the staged operative approach.
Fistula A fistula may be external or internal. The most common internal fistula is a colovesical fistula in the male. In a man with diverticulitis the colon usually becomes adherent to the bladder. If the inflammation continues it can lead to a colovesical fistula. For this reason, dysuria is an ominous sign in a man with diverticulitis. Sometimes the patient does not become alarmed until he begins to pass gas from his penis. When this occurs a fistula is already present. In a woman, a fistula is more likely to develop between the colon and vagina. This is particularly true if a hysterectomy has been performed. In some instances a one-stage resection with primary anastomosis can safely be performed when a complication of diverticulitis is present, such as a small and well localized perforation. With care and a good suction apparatus, contamination of the peritoneal cavity is unlikely. A one-stage resection can be done if an obstruction is only partial and the colon is not greatly distended. A one-stage resection can also be carried out if the inflammatory reaction surrounding a fistula is not extensive. It should never be done, however, without a careful evaluation of the risks involved. We should never forget that, when properly carried out, the multiple-stage approach is associated with almost no mortality and very few complications.
INDICATIONS FOR SURGERY IN DIVERTICULITIS
789
Hemorrhage In our experience, severe, persistent bleeding is a rare indication for surgery in patients with diverticulitis. Profuse bleeding is not common and when it does occur it will usually respond to conservative treatment. It may occur in patients who have diverticulosis with little or no diverticulitis. In none of the 150 patients operated on between 1950 and 1960 was bleeding the reason for surgical intervention. Many of these patients had had gross rectal bleeding but even in these patients, another cause for the bleeding-adenomatous polyps or large internal hemorrhoids-was often present. Indeed, a history of rectal bleeding in a patient with a localized lesion of the sigmoid colon should make the surgeon think first of cancer. *
Exclusion of Cancer A careful review of the history, the physical findings, and the barium enema study will rule out cancer in most patients. In a few patients, however, the duration of symptoms will be brief, the febrile reaction will be minimal and rectal bleeding may be frequent. If the barium enema study is equivocal, these patients must be operated on without further delay. Even with the abdomen open the surgeon may not be able to exclude cancer. He must then resect the bowel and its mesentery as he would for carcinoma. This will make the operative procedure more difficult and the likelihood of postoperative complications greater, but the surgeon has no choice. To treat such a patient for months, or to do a limited segmental resection in the belief that the lesion is just diverticulitis, may cost the patient his life.
Recurrent or Persistent Diverticulitis The time has come for surgeons to accept the challenge of reducing the morbidity as well as the mortality of the surgical treatment of diverticulitis. This can be done in two ways. First, operative procedures which are unsatisfactory for the treatment of this disease should be eliminated. Incision and drainage of an abscess resulting from a perforation usually produces a fecal fistula. The same is true for excision of a diverticulum or suture of a fistulous opening. Closure of the colostomy without resection of the diseased bowel usually ends in a recurrence of symptoms and often of the complication. We have seen patients who have had seven or eight operative procedures on their colon, but the complication of diverticulitis that they started with was still present. It is obvious, however, that even when the procedure is applied correctly, the morbidity of the surgical treatment of complicated diverticulitis is high. It will remain high as long as the surgical approach is delayed until perforation or obstruction occurs or a fistula develops. The finding of
* Colcock, B. P. and Sass, R. E.: Diverticulitis and carcinoma of the colon; differential diagnosis. Surg. Gynec. and Obst. 99: 627-633 (Nov.) 1954.
790
BENTLEY
P.
COLCOCK
diverticulosis without symptoms is not an indication for surgery. Mild discomfort in the left lower quadrant when diverticulosis is present may be entirely the result of an irritable colon. When the pain is recurrent and is associated with some fever, it probably indicates the development of diverticulitis. The same is true for the patient with left lower quadrant pain and a palpable mass. When these symptoms persist or increase in severity, elective resection of the diseased bowel should be seriously considered. In patients who have a significantly narrowed sigmoid on barium enema examination, complete obstruction may develop with their next attack. Dysuria in a patient with diverticulitis often precedes a colovesical fistula. I feel that any patient who has had two or more acute attacks (severe enough to suggest a small perforation) should have an operation. These patients are three times as likely to have a serious complication as is the patient who has had but one attack of diverticulitis. All of these complications are more frequent in patients who are under 55 years of age. Thus, to a large extent, we can recognize those patients with diverticulitis who are likely to have a complication of the disease. If they are operated on when the inflammatory reaction is well localized and the bowel is not distended, the morbidity of this disease can be greatly reduced. They require but one operation, and spend less than two weeks in the hospital. They require a minimum of medical and nursing care and are rarely out of work for more than six weeks. They are permanently relieved of their symptoms and they avoid the dangers of a serious complication. Most important of all, this can be done with a very low operative risk. No deaths occurred in this group of 150 patients operated on for diverticulitis between 1950 and 1960 even though 70 per cent had but one operation. It is only when the surgeon attempts the one-stage resection in patients with an extensive inflammatory process, or with a greatly distended bowel, that he is likely to run into difficulty.
SUMMARY
Diverticulitis may lead to three serious complications: perforation of the colon, obstruction of the colon, or a fecal fistula. When this happens, the first responsibility of the surgeon is to save that patient's life. This can be done by a well-planned, multiple-stage, operative procedure. Such a patient will survive, but he will also spend many weeks in the hospital. Two, and possibly three operations will be required and the patient must have a colostomy for several months. This can be avoided by operating on patients with persistent or recurrent diverticulitis before these complications develop. They can then be permanently relieved of their symptoms by one operation and will spend less than two weeks in the hospital. Also, the tragic result of allowing a carcinoma of the colon to go untreated is avoided. The operative risk at this stage is less than 1 per cent.