Original Article
Treatment of 171 Patients with Pulmonary Tuberculosis Resistant to Isoniazid and Rifampin
N Engl J Med 1993; 328:527-532February 25, 1993
- Abstract
Background and Methods
The frequency of infection with multidrug-resistant Mycobacterium tuberculosis is increasing. We reviewed the clinical courses of 171 patients with pulmonary disease due to M. tuberculosis resistant to rifampin and isoniazid who were referred to our hospital between 1973 and 1983. The patients' records were analyzed retrospectively. Their regimens were selected individually and preferably included three medications that they had not been given previously and to which the strain was fully susceptible.
Results
The 171 patients (median age, 46 years) had previously received a median of six drugs and shed bacilli that were resistant to a median of six drugs. Thus, their regimens were frequently not optimal. Of 134 patients with sufficient follow-up data, 87 (65 percent) responded to chemotherapy (as indicated by negative sputum cultures for at least three consecutive months); 47 patients (35 percent) had no response, as shown by continually positive cultures. The median stay in the hospital was more than seven months. In a multivariate analysis, an unfavorable response was significantly associated with a greater number of drugs received before the current course of therapy (odds ratio, 4.0; 95 percent confidence interval, 1.6 to 9.9; P<0.001) and with male sex (odds ratio, 2.5; 95 percent confidence interval, 1.1 to 6.2; P<0.03). Twelve of the patients with responses subsequently had relapses. The overall response rate was 56 percent over a mean period of 51 months. Of the 171 patients, 63 (37 percent) died, and 37 of these deaths were attributed to tuberculosis.
Conclusions
For patients with pulmonary tuberculosis that is resistant to rifampin and isoniazid, even the best available treatment is often unsuccessful. Only about half of such patients eventually have negative sputum cultures despite carefully selected regimens administered for extended periods. Failure to control this resistant infection is associated with high mortality and ominous implications for the public health.
Media in This Article
Figure 1
Drug Resistance of M. tuberculosis in 171 Patients on Admission.Figure 2
Survival of 134 Patients with Tuberculosis Resistant to Isoniazid and Rifampin, from the Initiation of Study Therapy to Death or the Most Recent Follow-up Examination.Article Activity
- Article
Modern chemotherapy, appropriately prescribed and administered, cures 98 to 99 percent of cases of previously untreated pulmonary tuberculosis if the disease is caused by drug-susceptible Mycobacterium tuberculosis1. Tubercle bacilli not previously exposed to antituberculosis drugs may manifest drug resistance as a result of random mutation2. Whereas such resistance can be overcome by appropriate multiple-drug regimens, inadequate antimicrobial therapy can lead to the emergence of drug-resistant strains. These resistant bacilli can in turn be passed on to previously uninfected persons, who may subsequently contract tuberculosis that is initially drug-resistant. Early in the chemotherapeutic era, 1 to 3 percent of patients were noted to have drug-resistant organisms, typically resistant to a single drug3,4. During the period 1982 through 1986, however, 8.8 percent of previously untreated patients in the United States were excreting M. tuberculosis resistant to at least one antituberculosis drug, and 23 percent of previously treated patients were shedding tubercle bacilli resistant to one or more medications5.
The majority of cases of resistance involve resistance to isoniazid and streptomycin. Until recently, resistance to rifampin has been relatively infrequent6. Introduced in the United States in 1971, rifampin has been prescribed widely, and resistance to it has emerged. Resistance to this drug was found in 0.6 percent of strains from previously untreated patients and 3.3 percent of strains from previously treated patients in the United States during the period 1982 through 19865. Some regions of the country have a higher prevalence of resistance7,8.
Resistance to rifampin is of extraordinary importance in modern chemotherapy. Rifampin and isoniazid are clearly the two most active antituberculosis drugs. The availability of rifampin allows successful and well-tolerated treatment in patients with organisms resistant to isoniazid, streptomycin, or other agents9-12. However, when resistance to rifampin occurs in the presence of resistance to isoniazid, the prospects for successful chemotherapy are greatly diminished6. In the United States, several outbreaks of tuberculosis due to strains resistant to isoniazid, rifampin, and other agents have recently been reported, in both patients with and patients without infection with the human immunodeficiency virus (HIV)13-15.
We present here our experience in treating a large series of patients with pulmonary tuberculosis resistant to both rifampin and isoniazid, and we discuss factors influencing outcomes and the implications for both the individual patient and the future of tuberculosis control.
Methods
The records of 231 patients hospitalized at our institution between January 1, 1973, and December 31, 1983, with pulmonary tuberculosis due to drug-resistant M. tuberculosis were reviewed retrospectively. All 171 patients shedding M. tuberculosis resistant to rifampin are discussed in this report. One of us was actively involved in the direct care of these patients at the center during the entire study period.
Susceptibility testing of all M. tuberculosis strains was performed in our laboratory on 7H11 agar according to standard proportionality techniques2. Resistance was indicated by the growth of more than 1 percent of the colonies on drug-containing medium, as compared with growth on drug-free (control) medium (Table 1Table 1
Concentrations of Drugs Tested and Dosages Administered in 171 Patients with Tuberculosis.). A drug was designated as “previously unused” if given for less than three months. Individually tailored regimens16,17 were selected for the patients on the basis of the results of in vitro susceptibility tests and the limited previous use or the nonuse of the drugs. The drugs and the dosages used are listed in Table 1. When possible, we administered three drugs not given previously to which the tubercle bacilli were fully susceptible at the lowest concentration tested in vitro, including one parenteral agent (an aminoglycoside or polypeptide) and two oral agents that met these criteria. Since many patients did not have such a regimen available to them, we also used drugs to which the organisms were at least partially susceptible (no growth at the higher concentrations tested, or 2 to 33 percent of control value for growth at the lowest concentration) or drugs previously given for a relatively short time; because of a lack of confidence in the full efficacy of drugs so selected, more than three medications were included in these regimens. The 171 patients received a median of four drugs; 32 patients received six or more drugs.To ensure compliance, nurses observed the patients while they took their medications. Ethionamide, pyrazinamide, aminosalicylic acid (para-amino salicylate), and cycloserine were given in divided doses to increase drug tolerance. Great efforts were made to continue therapy even if adverse drug reactions other than those considered life-threatening occurred. Patients usually remained in the hospital until a series of sputum cultures remained negative for at least three months or until treatment failure was evident after at least three months of therapy, as shown by continually positive sputum cultures. Success was indicated by three consecutive months of consistently negative cultures. While the patients were hospitalized, spontaneous or induced sputum specimens were examined every one to two weeks by fluorochrome staining of the concentrated specimen and culture on 7H11 agar and Lowenstein-Jensen medium. If patients resumed shedding tubercle bacilli after their cultures had been negative for three consecutive months, they were considered to have relapsed, whether or not they were still receiving therapy. After hospitalization, they returned to the care of the referring physician or agency, with the recommendation that oral antimycobacterial therapy should continue for at least two years after the last positive culture and that injectable antibiotics be given for four to six months after the initial date of culture conversion.
For this analysis, data on all 171 patients were reviewed, including identifying information, potential risk factors (alcoholism, bronchopleural fistula, cancer, diabetes, emphysema, fungal disease, gastrectomy, use of immunosuppressive drugs, interstitial lung disease, lung surgery, and silicosis), previous therapy with drugs given for at least three months, the referring agency's assessment of compliance, the results of in vitro susceptibility testing by direct or indirect methods of isolates obtained before the start of the new regimen, antituberculosis drugs initially administered at our hospital, drugs discontinued because of adverse effects, and the results of pretreatment smears and cultures and of the first sputum smear and culture obtained during each month of therapy. Adverse drug reactions not requiring the permanent discontinuation of a drug were not tabulated. In many cases, follow-up information was obtained from questionnaires sent to the physicians last known to be caring for the patients.
Statistical Analysis
To test for relations between outcome and each of several possible predictor variables, odds ratios with 95 percent confidence intervals were calculated separately for each variable18. When a variable had more than two categories, the odds ratio was calculated with respect to the lowest (reference) category. All these variables were entered into a stepwise logistic-regression model with use of SAS software with the Proc Logistic procedure19. The survival distribution was estimated with the Kaplan-Meier method in the SAS Proc Lifetest. This method includes the information on the subjects who were lost to follow-up or who died of causes other than tuberculosis during the time they were observed.
Results
Demographic Characteristics
The 171 patients with drug-resistant pulmonary tuberculosis were referred from 37 states and 5 foreign countries after treatment by physicians in their own communities had failed. Forty-eight were women, and 123 were men; their ages ranged from 17 to 79 years (median, 46). Ninety-six were white, 26 black, 29 Hispanic, 17 Asian, and 3 Native American.
Disease Characteristics
The patients had had tuberculosis for a median of 6 years (range, 1 to 39) and had received a median of 6 antituberculosis drugs (range, 2 to 11) before coming to our institution: 167 had previously received isoniazid, 163 rifampin, 163 ethambutol, 137 streptomycin, 107 pyrazinamide, 93 aminosalicylic acid, 76 cycloserine, 68 ethionamide, 47 capreomycin, 41 kanamycin, 17 viomycin, and 2 amikacin. The disease generally was advanced; 144 patients (84 percent) had bilateral disease with at least one cavity, and 126 (74 percent) had one or more organisms per field (x40) in concentrated sputum smears. All patients were shedding tubercle bacilli with resistance to a median of six drugs, including rifampin (Figure 1Figure 1
Drug Resistance of M. tuberculosis in 171 Patients on Admission.). All strains but one were also resistant to isoniazid; this strain occurred in a patient with severe toxic reactions that precluded the use of isoniazid.Emergence of Resistance to Rifampin
In 119 (70 percent) of the 171 patients with rifampin-resistant tubercle bacilli, the acquisition of the resistance was apparently associated with irregular administration of medications (which was due in 74 cases to documented noncompliance and in 12 to adverse reactions to medications), the administration of rifampin as the single effective agent, or both factors. In 43 cases, rifampin was added as a single drug to a failing regimen. In 16 cases, one new drug, rifampin, was added when treatment was resumed after noncompliance; in 2 cases, patients with tubercle bacilli initially resistant to isoniazid were treated with a regimen of only isoniazid and rifampin.
A less common factor was poor absorption of medications, which probably contributed to the emergence of resistance to rifampin in two additional patients who had previously undergone abdominal surgery (ileocolostomy in one and gastrojejunostomy in the other). Other factors that may have contributed to the emergence of resistance in 18 other patients included very extensive tuberculosis (12 patients), bronchopleural fistula (3), diabetes mellitus (2), and gastrectomy (1). During their initial medical encounter before referral to our center, three patients presented with organisms already resistant to rifampin, including two nurses who presumably acquired these organisms from patients for whom they were caring. Factors relating to the emergence of resistance to rifampin could not be identified in 29 patients.
Duration of Hospitalization
The median stay in the hospital was 7.3 months for patients whose treatment was successful and 7.8 months for those whose treatment failed.
Adverse Reactions
Fifty-one (30 percent) of 171 patients had adverse reactions that led to the discontinuation of one or more antimycobacterial medications (Table 2Table 2
Drug Toxicity Leading to Withdrawal of Treatment.). Twenty of these patients had serious toxic reactions to one or more drugs during the first three months of therapy.Adjunctive Surgery
Nine patients underwent surgical procedures as an adjunct to their antituberculosis chemotherapy. Three patients underwent right upper lobectomy, two left upper lobectomy, and two left pneumonectomy. The sputum cultures of all of these seven subsequently became negative. (Two patients had consistently negative cultures before surgery and were considered to have responded to chemotherapy, three had decreases in the number of tubercle bacilli in their sputum, and two had no bacteriologic response to chemotherapy alone.) The cultures of the two other patients remained positive; one patient underwent surgery to collapse a left-upper-lobe cavity with paraffin plombage, and in the other patient an Eloesser flap was created for drainage. The only surgical complication was a bronchopleural fistula, which resolved spontaneously by two months after the operation.
Exclusions from the Outcome Analysis
Of the 171 patients, 37 were excluded from the analysis of the outcome of chemotherapy for the following reasons: 8 died after receiving therapy for two months or less; 22 were lost to follow-up before they were observed long enough during chemotherapy; 3 did not meet the criterion of three months of negative sputum cultures before surgical resection, although they had had favorable responses; 1 deferred definitive therapy because of pregnancy; and 3 had had no positive cultures within the month before therapy started.
Outcomes of Chemotherapy
One hundred thirty-four patients were eligible for the analysis of the outcomes of chemotherapy. The sputum cultures of 87 of these patients (65 percent) became negative. The interval from the beginning of therapy to the first of a series of negative cultures ranged from one to eight months (median, two). Treatment failure, defined as the inability of chemotherapy to sterilize cultures, occurred in 47 patients (35 percent). Of the 87 patients who originally had negative cultures, 12 (14 percent) had relapses 5 to 62 months after the initiation of therapy, and 9 of these 12 had relapses within the first 2 years. Overall, 75 patients (56 percent) remained free of disease throughout a mean follow-up period of 51 months (range, 10 to 167), and 59 patients (44 percent) had unfavorable outcomes.
Deaths
Death due to tuberculosis occurred in 27 of the 59 patients (46 percent) with treatment failure or a relapse. The mean interval from the initial diagnosis to death was 11 years (median, 13), and the mean age at death was 52 years (range, 26 to 74). Four other patients with treatment failure died of causes unrelated to tuberculosis. Of the 87 patients with successful treatment, 15 died during the follow-up period; 13 died of causes not related to tuberculosis, and 2 died of undetermined causes. The estimated survival of the patients who could be evaluated and for whom the cause of death was known is shown in Figure 2Figure 2
Survival of 134 Patients with Tuberculosis Resistant to Isoniazid and Rifampin, from the Initiation of Study Therapy to Death or the Most Recent Follow-up Examination.. Among the 37 patients excluded from the analysis of the outcomes of chemotherapy, 10 (27 percent) died of tuberculosis and 7 (19 percent) died of other causes during the follow-up period. Thus, a total of 63 of the 171 patients died.Factors Influencing Outcome
In univariate analyses, four factors were associated with the failure of drug therapy to sterilize sputum cultures: previous administration of more drugs, regimens including fewer previously unused drugs, in vitro resistance to more drugs, and male sex (this factor was marginally associated with failure) (Table 3Table 3
Predictors of Outcome of Chemotherapy in 134 Patients with Pulmonary Tuberculosis Resistant to Isoniazid and Rifampin.). When all the factors were included in a multivariate model, only sex (odds ratio, 2.5; 95 percent confidence interval, 1.1 to 6.2) and the number of drugs received previously (odds ratio, 4.0; 95 percent confidence interval, 1.6 to 9.9) were significantly associated with treatment failure (P<0.03 and P<0.001, respectively).Many regimens were employed. The most frequently used regimens consisted of combinations of pyrazinamide, ethionamide, cycloserine, and aminosalicylic acid with one of the injectable aminoglycoside or polypeptide antimicrobial agents. Because of the small numbers of patients in each group, the efficacy of individual regimens could not be analyzed.
Discussion
Treatment of patients with pulmonary tuberculosis due to M. tuberculosis resistant to rifampin, isoniazid, and other medications is complicated, risky, and of limited efficacy. Fully 46 percent of our patients with treatment failure or relapses died. Physicians and society must recognize that multidrug-resistant tuberculosis is an ominous, deadly disease.
Patients who are treated unsuccessfully but remain alive pose a major public health problem. They must be isolated because of the risk of transmitting virtually untreatable drug-resistant disease. Drug-resistant tubercle bacilli were once believed less likely to be spread to contacts because the virulence of these organisms was diminished. However, a recent report20 demonstrated that rates of infection (as detected with the tuberculin skin test) among contacts of patients with drug-resistant tuberculosis were comparable overall to those among susceptible persons. In fact, because of their prolonged shedding of tubercle bacilli, previously treated patients with drug resistance had higher numbers of tuberculin-positive contacts than patients without resistance. Epidemics have been reported in which disease, including fatal meningitis and highly destructive lung disease, has evolved among persons infected with these drug-resistant microbes13-15,21-23. Quarantine of patients with treatment failure in their homes is a potential remedy but is seldom achievable. Confinement of patients may protect others, but they must then bear the additional burdens of isolation and stigmatization.
Because the number of drugs available was limited, our regimens for retreatment frequently entailed the use of agents known to be toxic or difficult to tolerate. When side effects occurred that were not potentially life-threatening and substitution of another medication was not feasible, we made great efforts to coach the patient through the drug intolerance, using both symptomatic palliation and psychological support. This required familiarity with each of the medications, as well as a great deal of time in giving care. Nonetheless, our success rate (65 percent) in treating disease due to multidrug-resistant isolates was less favorable than the rates in some earlier series of patients given retreatment in the pre-rifampin era24-26. The poorer results in the current study may be due to the larger number of drugs to which the isolates from our patients were resistant.
In our study an unsuccessful response to the therapy prescribed was strongly associated with a greater number of drugs received previously and with male sex. The reason for the association with male sex is not readily apparent, but it may be related to behavioral as well as biologic factors. The association with previous treatment with a greater number of drugs emphasizes the importance of thoroughly studying the patient's treatment history. Suboptimal previous therapy leads to the development of in vitro resistance. Thus, if the patient has already received a large number of drugs, few agents will still be available to which the isolate will be susceptible, and the chances for successful outcome decline.
However, some patients received drugs to which their organisms were susceptible according to conventional testing, yet they did not respond clinically. This suggests that improved methods of susceptibility testing are needed to provide more useful laboratory guidelines for retreatment regimens. We are currently exploring the use of the rapid radiometric system (Bactec) to determine minimal inhibitory concentrations27,28 -- values that we anticipate will replace the traditional “critical concentration” determined in solid agar.
Surgical resection as an adjunct to antituberculosis therapy was performed in patients who had amenable lesions and who were being treated with medical regimens deemed unlikely to effect permanent control of their disease. We attempted to schedule surgery so that it could be performed when the mycobacterial count in sputum reached its expected nadir. Three patients with indeterminate responses to medical therapy and two without bacteriologic responses to chemotherapy were clearly helped by resection. In the other two patients, whose sputum cultures had already become negative, the benefit of surgery was less clear.
When rifampin was introduced in 1971, it represented a major advance in antituberculosis treatment, leading to both short-course chemotherapy1 and highly effective, well-tolerated management of tuberculosis due to isoniazid-resistant organisms10. However, as anticipated,29 resistance to rifampin has emerged in substantial numbers of patients, frequently in association with the previous use of rifampin in an inadequate regimen and with noncompliance. Noncompliance contributed to the development of resistance to rifampin in 74 of our patients (43 percent of this series of 171 patients), and was suspected in many more. Noncompliance with prescribed treatment is extremely common30. The most effective safeguard is the directly observed administration of medications. The treatment of patients with multidrug-resistant tuberculosis entails five to seven visits per week. The cost of retreatment of patients in whom treatment fails and resistance to rifampin emerges should be considered when the economics of a tuberculosis-control program are being evaluated31. Our very limited rates of success in treating multidrug-resistant disease raise serious concerns about the future of tuberculosis control. If we, with all our resources, can successfully treat less than 60 percent of such patients, what will happen in less ideal circumstances? To avoid squandering the potential effectiveness of rifampin because of noncompliance or inept prescribing, systematic efforts are required to preserve the potency of this crucial drug against tuberculosis.
This report includes patients first seen between 1973 and 1983. Thus, it is likely that few, if any, of these patients were infected with HIV. However, many patients who have contracted multidrug-resistant tuberculosis have HIV infection14,15; their response to treatment appears to be very poor, with high rates of treatment failure and mortality32. Their response to antituberculosis therapy may be suboptimal, even when the organisms are susceptible to the drugs used33,34. Thus, although we recommend similar strategies for the therapy of drug-resistant tuberculosis whether or not it accompanies HIV infection, the efficacy of such therapy in patients with HIV remains to be determined. New antimycobacterial agents are urgently needed to expand our therapeutic options for multidrug-resistant tuberculosis.
Supported in part by a grant from the American Lung Association of Colorado.
We are indebted to Drs. Roger Mitchell, Paul Davidson, Tom Moulding, James Cook, and Leonid Heifets (and staff) for suggestions; to John LaBrecque, Mark Gabriel, and Dr. David Ikle for computer and statistical assistance; to Barry Silverstein for graphics; and to LaJuana Simms, Kitty Gentry, Corine Eckman, and Sharon Forsberg for assistance in the preparation of the manuscript.
Source Information
From the Departments of Medicine (M.G., M.D.I., L.A.M., D.W., L.A., C.R.H.) and Biostatistics (L.A.), National Jewish Center for Immunology and Respiratory Medicine, Denver.
Address reprint requests to Dr. Goble at the National Jewish Center for Immunology and Respiratory Medicine, 1400 Jackson St. Annex, Rm. J203, Denver, CO 80206.
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