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Chronic infection of the costal cartilages after thoracic surgical procedures
Chronic infection of the costal cartilages after thoracic surgical procedures C. David Williams, M.D., Joseph N. Cunningham, M.D., Emily A. Falk, Ph.D., O. Wayne [sam, M.D., Randolph N. Chase, Jr., M.D., and Frank C. Spencer, M.D., New York, N. Y.
RrtunatelY, infection of the costal cartilages is now rare. At one time tuberculosis was a common cause, but this is now almost never seen. During the preparation of this report, fewer than ten publications concerning costochondritis were found in the American surgical literature in the past 30 years, well indicating the paucity of surgical experience. In this report, experiences with 7 patients who had chronic infection of the costal cartilages and sternum following thoracic surgical procedures at New York University are described. Involvement of the cartilages led to a chronic, indolent infection, completely resistant to nonoperative therapy. In 4 of the 7, the infection was partly or completely due to Candida albicans, a previously unreported etiologic agent. Case reports CASE 1. E. H., a 60-year-old physician with severe angina, had an uneventful triple coronary bypass performed. Following operation cardiac function was satisfactory, but there was persistent leukocytosis. Wound drainage first began on the thirteenth postoperative day, revealing a sinus tract communicating with the mediastinum. Topical irrigation was begun, first with neomycin and
From the Departments of Surgery and Medicine, New York University Medical Center, 550 First Ave., New York, N. Y. 10016. Received for publication June 14, 1973.
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later with kanamycin. Wound cultures grew Escherichia coli. Three days later the sternotomy was reopened for debridement, drainage, and placement of irrigation catheters. Only the lower part of the sternum was infected. Neomycinbacitracin irrigation was performed for 2 weeks, during which the patient became afebrile and all incisions healed. He was discharged I month after the initial operation. Three months later purulent drainage began near the middle of the sternotomy incision. At reoperation the sternotomy wires were removed and the infected areas debrided. He was then discharged on ampicillin therapy. Wound drainage persisted however near the fourth costal cartilage. One month later he was hospitalized for the third time, and debridement of the third and fourth costal cartilages was performed. He was subsequently discharged with a granulating wound which healed completely within 2 weeks. CASE 2. N. S., a 66-year-old woman, underwent an uneventful triple coronary bypass for disabling angina pectoris. Reoperation for cardiac tamponade was necessary 8 hours later. Subsequent convalescence was uneventful. She was discharged three weeks after operation with persistent leukocytosis but no symptoms. In the next few months she was intermittently seen as an outpatient because of pain and tenderness over the costal arch. There was no fever or localizing findings. However, 4\!2 months after operation, a draining sinus appeared near the xyphoid process, as well as from a chest tube site near the right costal arch. Bacteriologic culture isolated Staphylococcus albus. She was rehospitalized and treated with oxacillin therapy for 3 weeks. Pain and tenderness were present along
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the right costal arch, without erythema or swelling. Despite continued antibiotic therapy, there was limited improvement. Accordingly, 3 weeks after admission the entire right costal arch and xyphoid process were surgically removed. Extensive costochondritis involving the entire arch was found. A week later pain and tenderness over the left costal arch was noted. This eventually required complete removal of the left costal arch as well. Both wounds were allowed to granulate and subsequently closed completely except for one sinus tract near the fourth left costal cartilage. She was discharged 3 weeks after the operation but drainage continued from the sinus tract for 5 months, at which time a small fragment of cartilage was spontaneously extruded. The wound closed soon thereafter. The patient is now well except for localized discomfort in the epigastrium associated with the unstable costal arches. CASE 3. J. F., a 53-year-old man, underwent aortic valve replacement for advanced aortic stenosis and insufficiency. He had developed severe pulmonary hypertension (systolic pressure 80 mm. Hg ), and the estimated heart size was 800 to 1,000 grams. Four days later multiple arrhythmias required multiple cardioversions and closedchest massage. Thereafter a fever to 105° F. developed, and a tracheostomy was done. Initial antibiotic therapy was oxacillin, penicillin, and streptomycin. Subsequently, cephalothin and corticosteroid therapy was also given. Although the fever subsided, progressive dehiscence of the sternum occurred. Drainage appeared from the wound a week after operation, and a chest roentgenogram showed widening of the mediastinum. Bacteriologic culture of the fluid draining from the wound was sterile. The patient was operated upon again for closure of the sternal dehiscence. At this time no obvious infection was noted, but irrigation catheters were left in the mediastinum through which neomycin was continuously instilled for several days. Ampicillin was given systemically. Wound cultures then grew Staphylococcus a/bus. Again the sternum failed to heal and gradually dehisced. Surgical closure was performed a second time two weeks later. The basic problem was multiple fractures of the sternum, greatly contributing to the instability. Again neomycin was instilled into the mediastinum through catheters for several days. A week after this operation, cultures of the drainage fluid grew Candida albicans. For this reason amphotericin B was given both systemically and through mediastinal irrigation fluid. This therapy was continued intermittently for 2 months, after which Candida albicans could no longer be cultured in the drainage fluid. Recurrent arrhythmias frequently appeared during amphotericin administration. The sternal wound closed slowly by granulation and
became stable. Multiple abscesses periodically appeared at different times, 6, 11, and 15 weeks after operation, usually in association with wires about the sternum. They appeared as localized areas of tenderness with swelling and redness and were treated by removal of the underlying wires. Chloramphenicol was given on one occasion but was poorly tolerated and subsequently refused by the patient. He was eventually discharged 5 months after admission with a chronic draining wound that was managed with local dressings and systemic oxacillin. In the subsequent 11 months the wounds gradually contracted but did not close completely. Chronic drainage continued without systemic sepsis. Cultures repeatedly grew Candida albicans. Eleven months after discharge he was rehospitalized for further debridement. At operation sinus tracts leading to both costal arches and the fourth right costal cartilage were found. The right costal arch and the fourth right costal cartilage were removed completely, as was the fifth left costal cartilage. Most of the left costal arch was left in place with a collar of perichondrium surrounding the termination of the resected cartilage. Subsequently topical irrigation with 0.25 per cent acetic acid was used, during which all wounds healed properly except in the area where the left costal cartilage had been divided. This drained intermittently for the subsequent 8 months, cultures always remaining positive for Candida albicans. The patient is currently in good condition with a 1 em. sinus tract. He has moderate discomfort from excision of the right costal arch. In the future, resection of the left costal arch may become necessary. CASE 4. W. J., a 55-year-old man, underwent triple coronary bypass for long-standing angina pectoris. In the recovery room an acute arrhythmia required external cardiac massage, followed by prompt recovery of normal rhythm. This massage may have contributed to dehiscence of the sternum. His convalescence appeared uneventful except for persistent wound pain over the next 2 weeks. Drainage then appeared from the lower portion of the wound, with a sinus tract communicating with the mediastinum. Some instability of the sternum became apparent. This progressively increased, necessitating reoperation for reclosure of the sternum and insertion of mediastinal irrigation catheters. At this time bacteriologic cultures were negative. Neomycin irrigation of the mediastinum, 1.5 Grn. daily, was performed for 5 days, after which the catheters were removed. One week later purulent drainage appeared, containing Candida albicans for the first time. There was no fever, however, and the white blood cell count was normal. The wound drainage continued for 26 days, after which the involved sternum was debrided and the second costal
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cartilage was removed. This wound granulated well and was closed with a split-thickness skin graft 7 weeks later. However, the lower portion of this wound began to drain near the third and fourth costal cartilages. The patient was temporarily discharged from the hospital on a program of topical therapy with 0.25 per cent acetic acid, but he was readmitted 6 weeks later because of increased drainage from the left costal cartilages. At reoperation the third and fourth cartilages and part of the adjacent sternum were removed. Cultures again grew Candida albicans . Two weeks later this wound was also closed with a splitthickness graft. Several weeks later, because of marked instability of the chest wall, a full-thickness flap was rotated, resulting in complete healing of the area. CASE 5. E. H., a 63-year-old man with chronic coronary disease, was scheduled for triple coronary bypass. He unexpectedly developed cardiac arrest while being brought into the operating room on a stretcher. Intubation was quickly done, external cardiac massage initiated, and femorofemoral bypass instituted. The chest was then hurriedly prepared and opened. A double coronary bypass was performed with a good result, fortunately without any neurological injury. However, cardiac tamponade developed in the postoperative period, requiring reoperation. A tracheostomy was done at this time. Two weeks later, massive bleeding from a gastric ulcer necessitated emergency gastrectomy. Despite the serious complications he was recovering well until drainage appeared from the sternal wound at two different sites. Cultures grew Candida albicans. There was no fever, and the white blood cell count was normal. He was subsequently discharged 5 weeks after operation, with continuing drainage from the sternal sinus. He was readmitted 3 months later because of persistent drainage and localized discomfort along the left costal arch and sternum. The cultures remained positive for Candida albicans. At reoperation, part of the left costal arch was removed and the xyphoid process was debrided. At the point of division of the left costal arch, care was taken to leave a collar of perichondrium surrounding normal cartilage. This wound closed by granulation in 2 to 3 months. The drainage continued from the sternal wound, however, remaining positive for Candida albicans, occasionally Escherichia coli or Staphylococcus albus. Operation was again performed 4 months later, at which time the xyphoid process and the distal sternum were excised. All wounds gradually closed within 3 months and have subsequently remained healed. CASE 6. H. R., a 61-year-old man, was admitted after a routine chest roentgenogram disclosed an asymptomatic mediastinal mass. Subsequently a
sterile cyst was removed through a left posterolateral thoracotomy incision. His initial convalescence was uneventful but a wound infection became apparent 9 days after operation, with fever to 101 F. and a leukocytosis of 14,000. Initial cultures grew Enterococcus. The wound was opened widely and drained. Pseudomonas was first isolated from the wound cultures 3 weeks after operation and persisted on all subsequent cultures. He was discharged with a granulating wound 5 weeks after operation, but readmission was necessary 2 months later because of increasing pain and drainage at the anterior portion of the incision. At this time the first involvement of a costal cartilage, the fourth, was found. This was removed along with its sternal articulation after which the patient was again discharged within 3 weeks with a granulating wound. Three weeks later rehospitalization was again necessary because of pain and purulent drainage from the anterior portion of this incision. At operation, debridement of the sternum and removal of part of the fifth costal cartilage were necessary. Repeated local debridement was subsequently required. Carbinocillin and gentamycin were given systemically. Two months later a splitthickness graft was applied on the 5 by 8 ern, granulating wound with a good result. He was discharged with complete healing of the wound 2 weeks later. The man has subsequently remained well. CASE 7. E. M., a 58-year-old man. was hospitalized for rheumatic valvular disease. At operation, aortic and mitral valve replacement was done. Serious hemorrhage developed at the site of aortotomy, resulting in 7 hours of cardiopulmonary bypass and a total operating time of 12Y2 hours. Hemostasis was eventually obtained only by packing the root of the aorta with a sponge. This was electively removed at thoracotomy 3 days later, at which time a tracheostomy was also performed. The patient recovered surprisingly well and was discharged 1 month later. Readmission was necessary I week after his discharge, however, because of a fever of 104 F. The sternal incision was painful and slightly reddened. At surgical exploration, a chronic infection was found with Candida albicans on culture. Mediastinal irrigation with neomycin, bacitracin, and amphotericin B was done for several days. The patient became afebrile and the sternum healed, but a sinus remained near the xyphoid process. He was discharged 2 months after admission. Seven weeks later hospitalization was again necessary for jaundice and continuing drainage near the xyphoid process. Candida albicans was again cultured from the fluid. Two weeks later the wound was again debrided and all sternal wires were removed. Drainage later appeared 0
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where the upper wires had been removed, necessitating removal of part of the manubrium and the second and third costal cartilages. Eventually all wounds healed by granulation, and he was discharged 3 weeks after operation. He has subsequently remained well.
Discussion Etiology. The etiology of costochondritis has changed significantly in recent years. A few decades ago, tuberculosis was the most common cause. This was emphasized in a report by Moschcowitz' in 1918. Other causative organisms were Salmonella typhi and Actinomyces. As mentioned earlier, very few reports have been published in the past 30 years. In 1947 Maier" described 4 cases in which streptococci and staphylococci were additional causative organisms. In 1959, Pontius and colleagues' described infections from Pseudomonas and Escherichia coli. In recent years, Wray- and Reckler" both noted an increasing frequency of infections by Pseudomonas. The patients described in this report are unique in that 4 of the 7 had infection with Candida albicans. This organism is usually a noninvasive saprophyte but has become a more common pathogen, especially since the introduction of intravenous alimentation. However, none of the 7 patients described in this report received intravenous alimentation. The 7 cases in this report were analyzed in detail, for the senior author had seen only 1 patient with infection of a costal cartilage following thoracotomy in the preceding 15 years. About 2 years ago the method of closure of sternotomy incisions was modified to deliberately insert sutures through costal cartilages rather than simply around the sternum in the intercostal spaces. This was adopted to permit wide placement of sutures to prevent dehiscence of the sternum in patients with an anatomically narrow sternum or multiple fractures of the sternum. This technique was employed in all 6 of the patients in this report who had a sternotomy. In this regard Case 7 is of particular interest, for there was no involvement of cartilage until the sternum was
reopened because of mediastinitis from Candida. Following this operation, with placement of sutures through cartilage, chondritis appeared. In Cases 2 and 5, infection of cartilage probably resulted from insertion of a chest tube near a cartilage rather than in a more lateral position near bone. Subsequently, since insertion of wire sutures through cartilage has been stopped, no further instances of chondritis have been seen. A second factor probably contributing to infection was prophylactic administration of broad-spectrum antibiotics for a long period of time, which could permit the overgrowth of organisms such as Candida albicans. All patients in this series received prophylactic oxacillin therapy, begun at the time of operation. Other antibiotics were used at different times, depending upon the bacteriologic cultures. The third factor contributing to infection may be the mediastinal irrigation with neomycin for 5 to 10 days in 4 of the 7 cases. This was done on a prophylactic basis, by means of a previously described technique," in all 4 patients who were reoperated upon because of dehiscence of the sternum. Two patients initially had sterile cultures of mediastinal fluid, with Candida developing only after mediastinal irrigations. Three of the 4 later infected with Candida had irrigation to the mediastinum at one time. The 2 patients who initially had sterile mediastinal fluid were operated upon for dehiscence of the sternum from mechanical factors (external cardiac massage in Case 4 and repeated cardioversion in Case 3). Pathogenisis of chondritis. Cartilage is relatively avascular, as it does not contain blood vessels and derives its nutrition by diffusion from vessels in the surrounding perichondrium. When denuded of perichondrium, cartilage becomes an avascular foreign body that easily develops a chronic abscess. This avascularity of cartilage contributes both to the astonishing chronicity of infection when established and to the inability to obtain healing without surgical removal of the infected cartilage.
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Chondritis can develop from either pyogenic organisms or fungi. It has occurred as a direct result of a traumatic injury, as an extension of adjacent infection, or from a systemic infection.P-" It has developed only rarely after radical mastectomy or drainage of a subphrenic abscess.": a., An unusual tendency, recognized for many years, is for the process to spread to adjacent cartilages and even across the sternum to contralateral cartilages.' This pernicious tendency was seen in Cases 2, 3, 4, and 6. In Case 2, there was infection of only the right costal arch at first. In the next 4 months this spread across the xyphoid process to the left costal arch. This case is somewhat similar to one reported by Siler' 21 years ago. He described a patient in whom complete resection of infected cartilage was initially delayed and, ultimately, removal of the sternum and all twenty costal cartilages was required. Another of our patients (Case 4) eventually required resection of the second, third, and fourth costal cartilages, resulting in a massive chest wall defect that required a full-thickness rotation flap for coverage. Earlier complete resection of the infected cartilage should prevent such disastrous extensions. Clinical characteristics. The clinical manifestations vary markedly with the offending organism. With bacterial infection, the familiar signs of infection develop, with the skin overlying the infected cartilage becoming tender, reddened, and swollen. When the area is incised, copious pus with liquefaction of the involved cartilage is found. Drainage continues until the cartilage is completely removed. There may be systemic signs of sepsis with fever and leukocytosis. By contrast, with infection of a bacterium of low virulence (such as Staphylococcus albus) or a fungus, the clinical findings are quite different. They may be sparse, even absent. In some patients for weeks there was only local tenderness with no other findings. Case 2 is an example of chondritis from Staphylococcus albus. The infection was manifested only by mild pain in the chest wall for 4 months before drainage ap-
peared at the site of the previous chest tube drainage. By this time, however, the process had spread to both costal arches, necessitating their removal in an extensive operation. Another of our patients (Case 3) similarly required multiple operations. The lesion in the right costal arch and xyphoid process drained for 11 months without systemic signs, but during this time the left costal arch also became infected. In some cases infection began separately in both the sternum and the costal cartilages. In others infection began in the sternum and then invaded adjacent cartilages, but the reverse pattern was seen in only 1 case (Case 6). With chondritis from Candida albicans, operative findings are quite distinctive. The cartilage is partly liquefied and replaced with granulation tissue, loose in texture, light pink, and poorly vascularized. The wound drainage is scanty, thin, and slightly cloudy. Following removal of the cartilage and irrigation with 0.25 per cent acetic acid, the wound appearance changes markedly to firm, reddish, vascular granulation tissue. The outstanding feature of infections of cartilage is their chronici ty (Table I). In these 7 patients the average duration of illness was 10 months, the longest 24 months, and the shortest about 6 months. Morbidity was further complicated by the number of operations required for ultimate cure. In both Cases 3 and 4, six separate operations were required for drainage of abscesses, cartilage resection, and plastic reconstruction. One of the wounds is still not healed (Case 3) and may require resection of an additional cartilage. The enormous economic burden of such a chronic illness is obvious. An important consideration in therapy is that such chronicity may be prevented by more adequate and early therapy. Prevention and treatment Prevention. Carefully avoiding the placement of wire sutures through the costal cartilages during closure of a sternotomy incision would seem crucial. This seems the most likely explanation for the abrupt ap-
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Table I
Case No. 1
2 3 4 5 6 7
Site of infection
Predominant organism
Cartilages and sternum Costal cartilages Cartilages and sternum Cartilages and sternum Cartilages and sternum Cartilages and sternum Cartilages and sternum
Escherichia coli Staphylococcus albus Candida albicans Candida albicans Candida albicans Enterococcus and Pseudomonas Candida albicans
pearance of these complicated cases over a period of 2 years, in contrast to their rarity in the past. Insertion of chest tubes laterally near a bony rib, rather than medially near a cartilage, is also important. Prophylactic administration of broad-spectrum antibiotics for long periods of time obviously encourages the overgrowth of secondary organisms. Hence such antibiotics should be given for only brief periods. Similarly, irrigation of the mediastinum with neomycin seemed to facilitate the secondary invasion by Candida in some patients. It is preferable for mediastinal irrigation to be done with more specific antibiotics, perhaps not at all if there are no signs of infection at the time of dehiscence of the sternum. Treatment. Once the diagnosis of chondritis is made, the etiologic organism identified, and the appropriate antibiotic sensitivities discerned, complete surgical excision of the involved cartilage should be done promptly. Prolonged nonoperative therapy with antibiotics is not only futile but also risks the insidious spread of infection to adjacent cartilages. This point should be emphasized, for the paucity of clinical findings in some patients encourages delay in operation. Not a single patient in this group recovered without excision of the involved cartilage, despite intensive therapy with specific antibiotics for long periods of time. The need for prompt, total removal of infected cartilage has been recognized for a long time and was recommended as early as 1906 by Konig," but this treatment has
Duration of illness (mo.) 6Y2
11 >24 10 13 7 7
Additional operations
Mediastinal irrigation
3 3 6 6 2 2 3
Yes No Yes Yes No No Yes
been generally forgotten in recent decades because of the rare occurrence of chondritis. At one time excision of the perichondrium was recommended, but this seems unnecessary and leads to permanent instability of this area of the chest wall. Complete excision of the first four costal cartilages is well tolerated. However, the fifth through the tenth cartilages are in continuity in the costal arch, and complete removal is undesirable. An approach effective in some patients in this group was to excise subperichondrially both the infected cartilage and 1 to 2 cm. of adjacent normal cartilage, leaving a 1 em. collar of perichondrium which could close over the ends of the exposed normal cartilage. If infection persists, complete excision of the costal arch becomes necessary. A conservative approach was successful in Cases 5 but not in Case 3. Following cartilage excision, the wound should be left open for topical irrigation with 0.25 per cent acetic acid. This proved far more effective than irrigation with antibiotics, amphotericin B, or iodoform gauze. It was especially effective in the presence of Candida. Systemic antibiotics may be given if specific antibiotic therapy is available. Blind administration of broad-spectrum antibiotics seems unnecessary, possibly hazardous. Systemic therapy with amphotericin B was ineffective in 1 patient and probably should be avoided because of its serious toxicity unless there are signs of systemic spread of the fungus infection. Once infec-
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tion has subsided, the granulating wounds may be closed with skin grafts.
Summary Experiences with 7 patients who had chondritis, often with associated sternal osteomyelitis, are described. All patients eventually recovered, but the average duration of illness was 10 months. The infection was due to Candida albicans in 4 cases and to bacteria in 3. Six infections developed after sternotomy for cardiopulmonary bypass, while one occurred after a left thoracotomy for a mediastinal cyst. Seemingly the most probable cause was the insertion of sutures through costal cartilage at the time of closure of the sternotomy incision. Prolonged use of broadspectrum antibiotics, either systemically or with mediastinal irrigation, seemed to be an additional contributing factor. Several principles of therapy were defined. Cure could not be obtained until the infected cartilage was completely removed. Prolonged administration of antibiotics without operation was futile. A serious hazard in delaying operation, even though clinical signs of infection were unimpressive, was the tendency for the infection process to spread to adjacent costal cartilages, even across the sternum to the contralateral chest wall. Extensive removal of both costal arches was ultimately required in 2 patients.
When infected cartilage in the costal arch was removed, subperichondrial excision of 1 to 2 em, of adjacent normal cartilage, leaving a collar of perichondrium to cover the transected end of the cartilage, was successful in some patients and provides an alternative to initial total removal of the costal arch. REFERENCES
2 3 4
5
6
7 8
Moschcowitz, A. V.: The Treatment of Diseases of the Costal Cartilages, Ann. Surg. 68: 168, 1918. Maier, H. C.: Infections of the Costal Cartilages and Sternum, Surg. Gynecol. Obstet. 84: 1038, 1947. Pontius, J. G., Clagett, O. T., and McDonald, J. R.: Costal Chondritis and Perichondritis, Surgery 45: 852, 1959. Wray, T. M., Bryant, R. E., and Killen, D. A.: Sternal Osteomyelitis and Costochondritis After Median Sternotomy, J. THORAC. CARDIOVASC. SURG. 65: 227, 1973. Reekier, J. M., Flemma, R. J., and Pruitt, B. A.: Costal Chondritis: An Unusual Complication in the Burned Patient, J. Trauma 13: 76, 1973. Bryant, L. R., Spencer, F. c., and Trinkle, J. K.: Treatment of Median Sternotomy Infection by Mediastinal Irrigation With an Antibiotic Solution, Ann. Surg. 169: 914, 1969. Siler, V. E.: Acute Costal Chondritis Associated With Sternal Osteomyelitis, Surgery 12: 407, 1942. Konig, F.: Die Tuberculose der Thoraxwand mit besonderer Berucksichtigung der Rippentuberculose auf Grund klinicher Beobactung, Arch. Klin. Chir. 79: I, 1906.
RrtunatelY, infection of the costal cartilages is now rare. At one time tuberculosis was a common cause, but this is now almost never seen. During the preparation of this report, fewer than ten publications concerning costochondritis were found in the American surgical literature in the past 30 years, well indicating the paucity of surgical experience. In this report, experiences with 7 patients who had chronic infection of the costal cartilages and sternum following thoracic surgical procedures at New York University are described. Involvement of the cartilages led to a chronic, indolent infection, completely resistant to nonoperative therapy. In 4 of the 7, the infection was partly or completely due to Candida albicans, a previously unreported etiologic agent. Case reports CASE 1. E. H., a 60-year-old physician with severe angina, had an uneventful triple coronary bypass performed. Following operation cardiac function was satisfactory, but there was persistent leukocytosis. Wound drainage first began on the thirteenth postoperative day, revealing a sinus tract communicating with the mediastinum. Topical irrigation was begun, first with neomycin and
From the Departments of Surgery and Medicine, New York University Medical Center, 550 First Ave., New York, N. Y. 10016. Received for publication June 14, 1973.
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later with kanamycin. Wound cultures grew Escherichia coli. Three days later the sternotomy was reopened for debridement, drainage, and placement of irrigation catheters. Only the lower part of the sternum was infected. Neomycinbacitracin irrigation was performed for 2 weeks, during which the patient became afebrile and all incisions healed. He was discharged I month after the initial operation. Three months later purulent drainage began near the middle of the sternotomy incision. At reoperation the sternotomy wires were removed and the infected areas debrided. He was then discharged on ampicillin therapy. Wound drainage persisted however near the fourth costal cartilage. One month later he was hospitalized for the third time, and debridement of the third and fourth costal cartilages was performed. He was subsequently discharged with a granulating wound which healed completely within 2 weeks. CASE 2. N. S., a 66-year-old woman, underwent an uneventful triple coronary bypass for disabling angina pectoris. Reoperation for cardiac tamponade was necessary 8 hours later. Subsequent convalescence was uneventful. She was discharged three weeks after operation with persistent leukocytosis but no symptoms. In the next few months she was intermittently seen as an outpatient because of pain and tenderness over the costal arch. There was no fever or localizing findings. However, 4\!2 months after operation, a draining sinus appeared near the xyphoid process, as well as from a chest tube site near the right costal arch. Bacteriologic culture isolated Staphylococcus albus. She was rehospitalized and treated with oxacillin therapy for 3 weeks. Pain and tenderness were present along
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the right costal arch, without erythema or swelling. Despite continued antibiotic therapy, there was limited improvement. Accordingly, 3 weeks after admission the entire right costal arch and xyphoid process were surgically removed. Extensive costochondritis involving the entire arch was found. A week later pain and tenderness over the left costal arch was noted. This eventually required complete removal of the left costal arch as well. Both wounds were allowed to granulate and subsequently closed completely except for one sinus tract near the fourth left costal cartilage. She was discharged 3 weeks after the operation but drainage continued from the sinus tract for 5 months, at which time a small fragment of cartilage was spontaneously extruded. The wound closed soon thereafter. The patient is now well except for localized discomfort in the epigastrium associated with the unstable costal arches. CASE 3. J. F., a 53-year-old man, underwent aortic valve replacement for advanced aortic stenosis and insufficiency. He had developed severe pulmonary hypertension (systolic pressure 80 mm. Hg ), and the estimated heart size was 800 to 1,000 grams. Four days later multiple arrhythmias required multiple cardioversions and closedchest massage. Thereafter a fever to 105° F. developed, and a tracheostomy was done. Initial antibiotic therapy was oxacillin, penicillin, and streptomycin. Subsequently, cephalothin and corticosteroid therapy was also given. Although the fever subsided, progressive dehiscence of the sternum occurred. Drainage appeared from the wound a week after operation, and a chest roentgenogram showed widening of the mediastinum. Bacteriologic culture of the fluid draining from the wound was sterile. The patient was operated upon again for closure of the sternal dehiscence. At this time no obvious infection was noted, but irrigation catheters were left in the mediastinum through which neomycin was continuously instilled for several days. Ampicillin was given systemically. Wound cultures then grew Staphylococcus a/bus. Again the sternum failed to heal and gradually dehisced. Surgical closure was performed a second time two weeks later. The basic problem was multiple fractures of the sternum, greatly contributing to the instability. Again neomycin was instilled into the mediastinum through catheters for several days. A week after this operation, cultures of the drainage fluid grew Candida albicans. For this reason amphotericin B was given both systemically and through mediastinal irrigation fluid. This therapy was continued intermittently for 2 months, after which Candida albicans could no longer be cultured in the drainage fluid. Recurrent arrhythmias frequently appeared during amphotericin administration. The sternal wound closed slowly by granulation and
became stable. Multiple abscesses periodically appeared at different times, 6, 11, and 15 weeks after operation, usually in association with wires about the sternum. They appeared as localized areas of tenderness with swelling and redness and were treated by removal of the underlying wires. Chloramphenicol was given on one occasion but was poorly tolerated and subsequently refused by the patient. He was eventually discharged 5 months after admission with a chronic draining wound that was managed with local dressings and systemic oxacillin. In the subsequent 11 months the wounds gradually contracted but did not close completely. Chronic drainage continued without systemic sepsis. Cultures repeatedly grew Candida albicans. Eleven months after discharge he was rehospitalized for further debridement. At operation sinus tracts leading to both costal arches and the fourth right costal cartilage were found. The right costal arch and the fourth right costal cartilage were removed completely, as was the fifth left costal cartilage. Most of the left costal arch was left in place with a collar of perichondrium surrounding the termination of the resected cartilage. Subsequently topical irrigation with 0.25 per cent acetic acid was used, during which all wounds healed properly except in the area where the left costal cartilage had been divided. This drained intermittently for the subsequent 8 months, cultures always remaining positive for Candida albicans. The patient is currently in good condition with a 1 em. sinus tract. He has moderate discomfort from excision of the right costal arch. In the future, resection of the left costal arch may become necessary. CASE 4. W. J., a 55-year-old man, underwent triple coronary bypass for long-standing angina pectoris. In the recovery room an acute arrhythmia required external cardiac massage, followed by prompt recovery of normal rhythm. This massage may have contributed to dehiscence of the sternum. His convalescence appeared uneventful except for persistent wound pain over the next 2 weeks. Drainage then appeared from the lower portion of the wound, with a sinus tract communicating with the mediastinum. Some instability of the sternum became apparent. This progressively increased, necessitating reoperation for reclosure of the sternum and insertion of mediastinal irrigation catheters. At this time bacteriologic cultures were negative. Neomycin irrigation of the mediastinum, 1.5 Grn. daily, was performed for 5 days, after which the catheters were removed. One week later purulent drainage appeared, containing Candida albicans for the first time. There was no fever, however, and the white blood cell count was normal. The wound drainage continued for 26 days, after which the involved sternum was debrided and the second costal
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cartilage was removed. This wound granulated well and was closed with a split-thickness skin graft 7 weeks later. However, the lower portion of this wound began to drain near the third and fourth costal cartilages. The patient was temporarily discharged from the hospital on a program of topical therapy with 0.25 per cent acetic acid, but he was readmitted 6 weeks later because of increased drainage from the left costal cartilages. At reoperation the third and fourth cartilages and part of the adjacent sternum were removed. Cultures again grew Candida albicans . Two weeks later this wound was also closed with a splitthickness graft. Several weeks later, because of marked instability of the chest wall, a full-thickness flap was rotated, resulting in complete healing of the area. CASE 5. E. H., a 63-year-old man with chronic coronary disease, was scheduled for triple coronary bypass. He unexpectedly developed cardiac arrest while being brought into the operating room on a stretcher. Intubation was quickly done, external cardiac massage initiated, and femorofemoral bypass instituted. The chest was then hurriedly prepared and opened. A double coronary bypass was performed with a good result, fortunately without any neurological injury. However, cardiac tamponade developed in the postoperative period, requiring reoperation. A tracheostomy was done at this time. Two weeks later, massive bleeding from a gastric ulcer necessitated emergency gastrectomy. Despite the serious complications he was recovering well until drainage appeared from the sternal wound at two different sites. Cultures grew Candida albicans. There was no fever, and the white blood cell count was normal. He was subsequently discharged 5 weeks after operation, with continuing drainage from the sternal sinus. He was readmitted 3 months later because of persistent drainage and localized discomfort along the left costal arch and sternum. The cultures remained positive for Candida albicans. At reoperation, part of the left costal arch was removed and the xyphoid process was debrided. At the point of division of the left costal arch, care was taken to leave a collar of perichondrium surrounding normal cartilage. This wound closed by granulation in 2 to 3 months. The drainage continued from the sternal wound, however, remaining positive for Candida albicans, occasionally Escherichia coli or Staphylococcus albus. Operation was again performed 4 months later, at which time the xyphoid process and the distal sternum were excised. All wounds gradually closed within 3 months and have subsequently remained healed. CASE 6. H. R., a 61-year-old man, was admitted after a routine chest roentgenogram disclosed an asymptomatic mediastinal mass. Subsequently a
sterile cyst was removed through a left posterolateral thoracotomy incision. His initial convalescence was uneventful but a wound infection became apparent 9 days after operation, with fever to 101 F. and a leukocytosis of 14,000. Initial cultures grew Enterococcus. The wound was opened widely and drained. Pseudomonas was first isolated from the wound cultures 3 weeks after operation and persisted on all subsequent cultures. He was discharged with a granulating wound 5 weeks after operation, but readmission was necessary 2 months later because of increasing pain and drainage at the anterior portion of the incision. At this time the first involvement of a costal cartilage, the fourth, was found. This was removed along with its sternal articulation after which the patient was again discharged within 3 weeks with a granulating wound. Three weeks later rehospitalization was again necessary because of pain and purulent drainage from the anterior portion of this incision. At operation, debridement of the sternum and removal of part of the fifth costal cartilage were necessary. Repeated local debridement was subsequently required. Carbinocillin and gentamycin were given systemically. Two months later a splitthickness graft was applied on the 5 by 8 ern, granulating wound with a good result. He was discharged with complete healing of the wound 2 weeks later. The man has subsequently remained well. CASE 7. E. M., a 58-year-old man. was hospitalized for rheumatic valvular disease. At operation, aortic and mitral valve replacement was done. Serious hemorrhage developed at the site of aortotomy, resulting in 7 hours of cardiopulmonary bypass and a total operating time of 12Y2 hours. Hemostasis was eventually obtained only by packing the root of the aorta with a sponge. This was electively removed at thoracotomy 3 days later, at which time a tracheostomy was also performed. The patient recovered surprisingly well and was discharged 1 month later. Readmission was necessary I week after his discharge, however, because of a fever of 104 F. The sternal incision was painful and slightly reddened. At surgical exploration, a chronic infection was found with Candida albicans on culture. Mediastinal irrigation with neomycin, bacitracin, and amphotericin B was done for several days. The patient became afebrile and the sternum healed, but a sinus remained near the xyphoid process. He was discharged 2 months after admission. Seven weeks later hospitalization was again necessary for jaundice and continuing drainage near the xyphoid process. Candida albicans was again cultured from the fluid. Two weeks later the wound was again debrided and all sternal wires were removed. Drainage later appeared 0
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where the upper wires had been removed, necessitating removal of part of the manubrium and the second and third costal cartilages. Eventually all wounds healed by granulation, and he was discharged 3 weeks after operation. He has subsequently remained well.
Discussion Etiology. The etiology of costochondritis has changed significantly in recent years. A few decades ago, tuberculosis was the most common cause. This was emphasized in a report by Moschcowitz' in 1918. Other causative organisms were Salmonella typhi and Actinomyces. As mentioned earlier, very few reports have been published in the past 30 years. In 1947 Maier" described 4 cases in which streptococci and staphylococci were additional causative organisms. In 1959, Pontius and colleagues' described infections from Pseudomonas and Escherichia coli. In recent years, Wray- and Reckler" both noted an increasing frequency of infections by Pseudomonas. The patients described in this report are unique in that 4 of the 7 had infection with Candida albicans. This organism is usually a noninvasive saprophyte but has become a more common pathogen, especially since the introduction of intravenous alimentation. However, none of the 7 patients described in this report received intravenous alimentation. The 7 cases in this report were analyzed in detail, for the senior author had seen only 1 patient with infection of a costal cartilage following thoracotomy in the preceding 15 years. About 2 years ago the method of closure of sternotomy incisions was modified to deliberately insert sutures through costal cartilages rather than simply around the sternum in the intercostal spaces. This was adopted to permit wide placement of sutures to prevent dehiscence of the sternum in patients with an anatomically narrow sternum or multiple fractures of the sternum. This technique was employed in all 6 of the patients in this report who had a sternotomy. In this regard Case 7 is of particular interest, for there was no involvement of cartilage until the sternum was
reopened because of mediastinitis from Candida. Following this operation, with placement of sutures through cartilage, chondritis appeared. In Cases 2 and 5, infection of cartilage probably resulted from insertion of a chest tube near a cartilage rather than in a more lateral position near bone. Subsequently, since insertion of wire sutures through cartilage has been stopped, no further instances of chondritis have been seen. A second factor probably contributing to infection was prophylactic administration of broad-spectrum antibiotics for a long period of time, which could permit the overgrowth of organisms such as Candida albicans. All patients in this series received prophylactic oxacillin therapy, begun at the time of operation. Other antibiotics were used at different times, depending upon the bacteriologic cultures. The third factor contributing to infection may be the mediastinal irrigation with neomycin for 5 to 10 days in 4 of the 7 cases. This was done on a prophylactic basis, by means of a previously described technique," in all 4 patients who were reoperated upon because of dehiscence of the sternum. Two patients initially had sterile cultures of mediastinal fluid, with Candida developing only after mediastinal irrigations. Three of the 4 later infected with Candida had irrigation to the mediastinum at one time. The 2 patients who initially had sterile mediastinal fluid were operated upon for dehiscence of the sternum from mechanical factors (external cardiac massage in Case 4 and repeated cardioversion in Case 3). Pathogenisis of chondritis. Cartilage is relatively avascular, as it does not contain blood vessels and derives its nutrition by diffusion from vessels in the surrounding perichondrium. When denuded of perichondrium, cartilage becomes an avascular foreign body that easily develops a chronic abscess. This avascularity of cartilage contributes both to the astonishing chronicity of infection when established and to the inability to obtain healing without surgical removal of the infected cartilage.
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Chondritis can develop from either pyogenic organisms or fungi. It has occurred as a direct result of a traumatic injury, as an extension of adjacent infection, or from a systemic infection.P-" It has developed only rarely after radical mastectomy or drainage of a subphrenic abscess.": a., An unusual tendency, recognized for many years, is for the process to spread to adjacent cartilages and even across the sternum to contralateral cartilages.' This pernicious tendency was seen in Cases 2, 3, 4, and 6. In Case 2, there was infection of only the right costal arch at first. In the next 4 months this spread across the xyphoid process to the left costal arch. This case is somewhat similar to one reported by Siler' 21 years ago. He described a patient in whom complete resection of infected cartilage was initially delayed and, ultimately, removal of the sternum and all twenty costal cartilages was required. Another of our patients (Case 4) eventually required resection of the second, third, and fourth costal cartilages, resulting in a massive chest wall defect that required a full-thickness rotation flap for coverage. Earlier complete resection of the infected cartilage should prevent such disastrous extensions. Clinical characteristics. The clinical manifestations vary markedly with the offending organism. With bacterial infection, the familiar signs of infection develop, with the skin overlying the infected cartilage becoming tender, reddened, and swollen. When the area is incised, copious pus with liquefaction of the involved cartilage is found. Drainage continues until the cartilage is completely removed. There may be systemic signs of sepsis with fever and leukocytosis. By contrast, with infection of a bacterium of low virulence (such as Staphylococcus albus) or a fungus, the clinical findings are quite different. They may be sparse, even absent. In some patients for weeks there was only local tenderness with no other findings. Case 2 is an example of chondritis from Staphylococcus albus. The infection was manifested only by mild pain in the chest wall for 4 months before drainage ap-
peared at the site of the previous chest tube drainage. By this time, however, the process had spread to both costal arches, necessitating their removal in an extensive operation. Another of our patients (Case 3) similarly required multiple operations. The lesion in the right costal arch and xyphoid process drained for 11 months without systemic signs, but during this time the left costal arch also became infected. In some cases infection began separately in both the sternum and the costal cartilages. In others infection began in the sternum and then invaded adjacent cartilages, but the reverse pattern was seen in only 1 case (Case 6). With chondritis from Candida albicans, operative findings are quite distinctive. The cartilage is partly liquefied and replaced with granulation tissue, loose in texture, light pink, and poorly vascularized. The wound drainage is scanty, thin, and slightly cloudy. Following removal of the cartilage and irrigation with 0.25 per cent acetic acid, the wound appearance changes markedly to firm, reddish, vascular granulation tissue. The outstanding feature of infections of cartilage is their chronici ty (Table I). In these 7 patients the average duration of illness was 10 months, the longest 24 months, and the shortest about 6 months. Morbidity was further complicated by the number of operations required for ultimate cure. In both Cases 3 and 4, six separate operations were required for drainage of abscesses, cartilage resection, and plastic reconstruction. One of the wounds is still not healed (Case 3) and may require resection of an additional cartilage. The enormous economic burden of such a chronic illness is obvious. An important consideration in therapy is that such chronicity may be prevented by more adequate and early therapy. Prevention and treatment Prevention. Carefully avoiding the placement of wire sutures through the costal cartilages during closure of a sternotomy incision would seem crucial. This seems the most likely explanation for the abrupt ap-
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Table I
Case No. 1
2 3 4 5 6 7
Site of infection
Predominant organism
Cartilages and sternum Costal cartilages Cartilages and sternum Cartilages and sternum Cartilages and sternum Cartilages and sternum Cartilages and sternum
Escherichia coli Staphylococcus albus Candida albicans Candida albicans Candida albicans Enterococcus and Pseudomonas Candida albicans
pearance of these complicated cases over a period of 2 years, in contrast to their rarity in the past. Insertion of chest tubes laterally near a bony rib, rather than medially near a cartilage, is also important. Prophylactic administration of broad-spectrum antibiotics for long periods of time obviously encourages the overgrowth of secondary organisms. Hence such antibiotics should be given for only brief periods. Similarly, irrigation of the mediastinum with neomycin seemed to facilitate the secondary invasion by Candida in some patients. It is preferable for mediastinal irrigation to be done with more specific antibiotics, perhaps not at all if there are no signs of infection at the time of dehiscence of the sternum. Treatment. Once the diagnosis of chondritis is made, the etiologic organism identified, and the appropriate antibiotic sensitivities discerned, complete surgical excision of the involved cartilage should be done promptly. Prolonged nonoperative therapy with antibiotics is not only futile but also risks the insidious spread of infection to adjacent cartilages. This point should be emphasized, for the paucity of clinical findings in some patients encourages delay in operation. Not a single patient in this group recovered without excision of the involved cartilage, despite intensive therapy with specific antibiotics for long periods of time. The need for prompt, total removal of infected cartilage has been recognized for a long time and was recommended as early as 1906 by Konig," but this treatment has
Duration of illness (mo.) 6Y2
11 >24 10 13 7 7
Additional operations
Mediastinal irrigation
3 3 6 6 2 2 3
Yes No Yes Yes No No Yes
been generally forgotten in recent decades because of the rare occurrence of chondritis. At one time excision of the perichondrium was recommended, but this seems unnecessary and leads to permanent instability of this area of the chest wall. Complete excision of the first four costal cartilages is well tolerated. However, the fifth through the tenth cartilages are in continuity in the costal arch, and complete removal is undesirable. An approach effective in some patients in this group was to excise subperichondrially both the infected cartilage and 1 to 2 cm. of adjacent normal cartilage, leaving a 1 em. collar of perichondrium which could close over the ends of the exposed normal cartilage. If infection persists, complete excision of the costal arch becomes necessary. A conservative approach was successful in Cases 5 but not in Case 3. Following cartilage excision, the wound should be left open for topical irrigation with 0.25 per cent acetic acid. This proved far more effective than irrigation with antibiotics, amphotericin B, or iodoform gauze. It was especially effective in the presence of Candida. Systemic antibiotics may be given if specific antibiotic therapy is available. Blind administration of broad-spectrum antibiotics seems unnecessary, possibly hazardous. Systemic therapy with amphotericin B was ineffective in 1 patient and probably should be avoided because of its serious toxicity unless there are signs of systemic spread of the fungus infection. Once infec-
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tion has subsided, the granulating wounds may be closed with skin grafts.
Summary Experiences with 7 patients who had chondritis, often with associated sternal osteomyelitis, are described. All patients eventually recovered, but the average duration of illness was 10 months. The infection was due to Candida albicans in 4 cases and to bacteria in 3. Six infections developed after sternotomy for cardiopulmonary bypass, while one occurred after a left thoracotomy for a mediastinal cyst. Seemingly the most probable cause was the insertion of sutures through costal cartilage at the time of closure of the sternotomy incision. Prolonged use of broadspectrum antibiotics, either systemically or with mediastinal irrigation, seemed to be an additional contributing factor. Several principles of therapy were defined. Cure could not be obtained until the infected cartilage was completely removed. Prolonged administration of antibiotics without operation was futile. A serious hazard in delaying operation, even though clinical signs of infection were unimpressive, was the tendency for the infection process to spread to adjacent costal cartilages, even across the sternum to the contralateral chest wall. Extensive removal of both costal arches was ultimately required in 2 patients.
When infected cartilage in the costal arch was removed, subperichondrial excision of 1 to 2 em, of adjacent normal cartilage, leaving a collar of perichondrium to cover the transected end of the cartilage, was successful in some patients and provides an alternative to initial total removal of the costal arch. REFERENCES
2 3 4
5
6
7 8
Moschcowitz, A. V.: The Treatment of Diseases of the Costal Cartilages, Ann. Surg. 68: 168, 1918. Maier, H. C.: Infections of the Costal Cartilages and Sternum, Surg. Gynecol. Obstet. 84: 1038, 1947. Pontius, J. G., Clagett, O. T., and McDonald, J. R.: Costal Chondritis and Perichondritis, Surgery 45: 852, 1959. Wray, T. M., Bryant, R. E., and Killen, D. A.: Sternal Osteomyelitis and Costochondritis After Median Sternotomy, J. THORAC. CARDIOVASC. SURG. 65: 227, 1973. Reekier, J. M., Flemma, R. J., and Pruitt, B. A.: Costal Chondritis: An Unusual Complication in the Burned Patient, J. Trauma 13: 76, 1973. Bryant, L. R., Spencer, F. c., and Trinkle, J. K.: Treatment of Median Sternotomy Infection by Mediastinal Irrigation With an Antibiotic Solution, Ann. Surg. 169: 914, 1969. Siler, V. E.: Acute Costal Chondritis Associated With Sternal Osteomyelitis, Surgery 12: 407, 1942. Konig, F.: Die Tuberculose der Thoraxwand mit besonderer Berucksichtigung der Rippentuberculose auf Grund klinicher Beobactung, Arch. Klin. Chir. 79: I, 1906.