Background and Methods The frequency of infection with multidrug-resistantMycobacterium tuberculosis is increasing. We reviewed the clinicalcourses of 171 patients with pulmonary disease due to M. tuberculosisresistant to rifampin and isoniazid who were referred to ourhospital between 1973 and 1983. The patients' records were analyzedretrospectively. Their regimens were selected individually andpreferably included three medications that they had not beengiven previously and to which the strain was fully susceptible.
Results The 171 patients (median age, 46 years) had previouslyreceived a median of six drugs and shed bacilli that were resistantto a median of six drugs. Thus, their regimens were frequentlynot optimal. Of 134 patients with sufficient follow-up data,87 (65 percent) responded to chemotherapy (as indicated by negativesputum cultures for at least three consecutive months); 47 patients(35 percent) had no response, as shown by continually positivecultures. The median stay in the hospital was more than sevenmonths. In a multivariate analysis, an unfavorable responsewas significantly associated with a greater number of drugsreceived before the current course of therapy (odds ratio, 4.0;95 percent confidence interval, 1.6 to 9.9; P<0.001) andwith male sex (odds ratio, 2.5; 95 percent confidence interval,1.1 to 6.2; P<0.03). Twelve of the patients with responsessubsequently had relapses. The overall response rate was 56percent over a mean period of 51 months. Of the 171 patients,63 (37 percent) died, and 37 of these deaths were attributedto tuberculosis.
Conclusions For patients with pulmonary tuberculosis that isresistant to rifampin and isoniazid, even the best availabletreatment is often unsuccessful. Only about half of such patientseventually have negative sputum cultures despite carefully selectedregimens administered for extended periods. Failure to controlthis resistant infection is associated with high mortality andominous implications for the public health.
Modern chemotherapy, appropriately prescribed and administered,cures 98 to 99 percent of cases of previously untreated pulmonarytuberculosis if the disease is caused by drug-susceptible Mycobacteriumtuberculosis1. Tubercle bacilli not previously exposed to antituberculosisdrugs may manifest drug resistance as a result of random mutation2.Whereas such resistance can be overcome by appropriate multiple-drugregimens, inadequate antimicrobial therapy can lead to the emergenceof drug-resistant strains. These resistant bacilli can in turnbe passed on to previously uninfected persons, who may subsequentlycontract tuberculosis that is initially drug-resistant. Earlyin the chemotherapeutic era, 1 to 3 percent of patients werenoted to have drug-resistant organisms, typically resistantto a single drug3,4. During the period 1982 through 1986, however,8.8 percent of previously untreated patients in the United Stateswere excreting M. tuberculosis resistant to at least one antituberculosisdrug, and 23 percent of previously treated patients were sheddingtubercle bacilli resistant to one or more medications5.
The majority of cases of resistance involve resistance to isoniazidand streptomycin. Until recently, resistance to rifampin hasbeen relatively infrequent6. Introduced in the United Statesin 1971, rifampin has been prescribed widely, and resistanceto it has emerged. Resistance to this drug was found in 0.6percent of strains from previously untreated patients and 3.3percent of strains from previously treated patients in the UnitedStates during the period 1982 through 19865. Some regions ofthe country have a higher prevalence of resistance7,8.
Resistance to rifampin is of extraordinary importance in modernchemotherapy. Rifampin and isoniazid are clearly the two mostactive antituberculosis drugs. The availability of rifampinallows successful and well-tolerated treatment in patients withorganisms resistant to isoniazid, streptomycin, or other agents9,10,11,12.However, when resistance to rifampin occurs in the presenceof resistance to isoniazid, the prospects for successful chemotherapyare greatly diminished6. In the United States, several outbreaksof tuberculosis due to strains resistant to isoniazid, rifampin,and other agents have recently been reported, in both patientswith and patients without infection with the human immunodeficiencyvirus (HIV)13,14,15.
We present here our experience in treating a large series ofpatients with pulmonary tuberculosis resistant to both rifampinand isoniazid, and we discuss factors influencing outcomes andthe implications for both the individual patient and the futureof tuberculosis control.
Methods
The records of 231 patients hospitalized at our institutionbetween January 1, 1973, and December 31, 1983, with pulmonarytuberculosis due to drug-resistant M. tuberculosis were reviewedretrospectively. All 171 patients shedding M. tuberculosis resistantto rifampin are discussed in this report. One of us was activelyinvolved in the direct care of these patients at the centerduring the entire study period.
Susceptibility testing of all M. tuberculosis strains was performedin our laboratory on 7H11 agar according to standard proportionalitytechniques2. Resistance was indicated by the growth of morethan 1 percent of the colonies on drug-containing medium, ascompared with growth on drug-free (control) medium (Table 1).A drug was designated as "previously unused" if given for lessthan three months. Individually tailored regimens16,17 wereselected for the patients on the basis of the results of invitro susceptibility tests and the limited previous use or thenonuse of the drugs. The drugs and the dosages used are listedin Table 1. When possible, we administered three drugs not givenpreviously to which the tubercle bacilli were fully susceptibleat the lowest concentration tested in vitro, including one parenteralagent (an aminoglycoside or polypeptide) and two oral agentsthat met these criteria. Since many patients did not have sucha regimen available to them, we also used drugs to which theorganisms were at least partially susceptible (no growth atthe higher concentrations tested, or 2 to 33 percent of controlvalue for growth at the lowest concentration) or drugs previouslygiven for a relatively short time; because of a lack of confidencein the full efficacy of drugs so selected, more than three medicationswere included in these regimens. The 171 patients received amedian of four drugs; 32 patients received six or more drugs.
Table 1. Concentrations of Drugs Tested and Dosages Administered in 171 Patients with Tuberculosis.
To ensure compliance, nurses observed the patients while theytook their medications. Ethionamide, pyrazinamide, aminosalicylicacid (para-amino salicylate), and cycloserine were given individed doses to increase drug tolerance. Great efforts weremade to continue therapy even if adverse drug reactions otherthan those considered life-threatening occurred. Patients usuallyremained in the hospital until a series of sputum cultures remainednegative for at least three months or until treatment failurewas evident after at least three months of therapy, as shownby continually positive sputum cultures. Success was indicatedby three consecutive months of consistently negative cultures.While the patients were hospitalized, spontaneous or inducedsputum specimens were examined every one to two weeks by fluorochromestaining of the concentrated specimen and culture on 7H11 agarand Lowenstein-Jensen medium. If patients resumed shedding tuberclebacilli after their cultures had been negative for three consecutivemonths, they were considered to have relapsed, whether or notthey were still receiving therapy. After hospitalization, theyreturned to the care of the referring physician or agency, withthe recommendation that oral antimycobacterial therapy shouldcontinue for at least two years after the last positive cultureand that injectable antibiotics be given for four to six monthsafter the initial date of culture conversion.
For this analysis, data on all 171 patients were reviewed, includingidentifying information, potential risk factors (alcoholism,bronchopleural fistula, cancer, diabetes, emphysema, fungaldisease, gastrectomy, use of immunosuppressive drugs, interstitiallung disease, lung surgery, and silicosis), previous therapywith drugs given for at least three months, the referring agency'sassessment of compliance, the results of in vitro susceptibilitytesting by direct or indirect methods of isolates obtained beforethe start of the new regimen, antituberculosis drugs initiallyadministered at our hospital, drugs discontinued because ofadverse effects, and the results of pretreatment smears andcultures and of the first sputum smear and culture obtainedduring each month of therapy. Adverse drug reactions not requiringthe permanent discontinuation of a drug were not tabulated.In many cases, follow-up information was obtained from questionnairessent to the physicians last known to be caring for the patients.
Statistical Analysis
To test for relations between outcome and each of several possiblepredictor variables, odds ratios with 95 percent confidenceintervals were calculated separately for each variable18. Whena variable had more than two categories, the odds ratio wascalculated with respect to the lowest (reference) category.All these variables were entered into a stepwise logistic-regressionmodel with use of SAS software with the Proc Logistic procedure19.The survival distribution was estimated with the Kaplan-Meiermethod in the SAS Proc Lifetest. This method includes the informationon the subjects who were lost to follow-up or who died of causesother than tuberculosis during the time they were observed.
Results
Demographic Characteristics
The 171 patients with drug-resistant pulmonary tuberculosiswere referred from 37 states and 5 foreign countries after treatmentby physicians in their own communities had failed. Forty-eightwere women, and 123 were men; their ages ranged from 17 to 79years (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 previouslyreceived isoniazid, 163 rifampin, 163 ethambutol, 137 streptomycin,107 pyrazinamide, 93 aminosalicylic acid, 76 cycloserine, 68ethionamide, 47 capreomycin, 41 kanamycin, 17 viomycin, and2 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 tuberclebacilli with resistance to a median of six drugs, includingrifampin (Figure 1). All strains but one were also resistantto isoniazid; this strain occurred in a patient with severetoxic reactions that precluded the use of isoniazid.
Figure 1. Drug Resistance of M. tuberculosis in 171 Patients on Admission.
Emergence of Resistance to Rifampin
In 119 (70 percent) of the 171 patients with rifampin-resistanttubercle bacilli, the acquisition of the resistance was apparentlyassociated with irregular administration of medications (whichwas due in 74 cases to documented noncompliance and in 12 toadverse reactions to medications), the administration of rifampinas the single effective agent, or both factors. In 43 cases,rifampin was added as a single drug to a failing regimen. In16 cases, one new drug, rifampin, was added when treatment wasresumed after noncompliance; in 2 cases, patients with tuberclebacilli initially resistant to isoniazid were treated with aregimen of only isoniazid and rifampin.
A less common factor was poor absorption of medications, whichprobably contributed to the emergence of resistance to rifampinin two additional patients who had previously undergone abdominalsurgery (ileocolostomy in one and gastrojejunostomy in the other).Other factors that may have contributed to the emergence ofresistance in 18 other patients included very extensive tuberculosis(12 patients), bronchopleural fistula (3), diabetes mellitus(2), and gastrectomy (1). During their initial medical encounterbefore referral to our center, three patients presented withorganisms already resistant to rifampin, including two nurseswho presumably acquired these organisms from patients for whomthey were caring. Factors relating to the emergence of resistanceto rifampin could not be identified in 29 patients.
Duration of Hospitalization
The median stay in the hospital was 7.3 months for patientswhose treatment was successful and 7.8 months for those whosetreatment failed.
Adverse Reactions
Fifty-one (30 percent) of 171 patients had adverse reactionsthat led to the discontinuation of one or more antimycobacterialmedications (Table 2). Twenty of these patients had serioustoxic reactions to one or more drugs during the first threemonths of therapy.
Table 2. Drug Toxicity Leading to Withdrawal of Treatment.
Adjunctive Surgery
Nine patients underwent surgical procedures as an adjunct totheir antituberculosis chemotherapy. Three patients underwentright upper lobectomy, two left upper lobectomy, and two leftpneumonectomy. The sputum cultures of all of these seven subsequentlybecame negative. (Two patients had consistently negative culturesbefore surgery and were considered to have responded to chemotherapy,three had decreases in the number of tubercle bacilli in theirsputum, and two had no bacteriologic response to chemotherapyalone.) The cultures of the two other patients remained positive;one patient underwent surgery to collapse a left-upper-lobecavity with paraffin plombage, and in the other patient an Eloesserflap was created for drainage. The only surgical complicationwas a bronchopleural fistula, which resolved spontaneously bytwo months after the operation.
Exclusions from the Outcome Analysis
Of the 171 patients, 37 were excluded from the analysis of theoutcome of chemotherapy for the following reasons: 8 died afterreceiving therapy for two months or less; 22 were lost to follow-upbefore they were observed long enough during chemotherapy; 3did not meet the criterion of three months of negative sputumcultures before surgical resection, although they had had favorableresponses; 1 deferred definitive therapy because of pregnancy;and 3 had had no positive cultures within the month before therapystarted.
Outcomes of Chemotherapy
One hundred thirty-four patients were eligible for the analysisof the outcomes of chemotherapy. The sputum cultures of 87 ofthese patients (65 percent) became negative. The interval fromthe beginning of therapy to the first of a series of negativecultures ranged from one to eight months (median, two). Treatmentfailure, defined as the inability of chemotherapy to sterilizecultures, occurred in 47 patients (35 percent). Of the 87 patientswho originally had negative cultures, 12 (14 percent) had relapses5 to 62 months after the initiation of therapy, and 9 of these12 had relapses within the first 2 years. Overall, 75 patients(56 percent) remained free of disease throughout a mean follow-upperiod of 51 months (range, 10 to 167), and 59 patients (44percent) 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 intervalfrom the initial diagnosis to death was 11 years (median, 13),and the mean age at death was 52 years (range, 26 to 74). Fourother patients with treatment failure died of causes unrelatedto tuberculosis. Of the 87 patients with successful treatment,15 died during the follow-up period; 13 died of causes not relatedto tuberculosis, and 2 died of undetermined causes. The estimatedsurvival of the patients who could be evaluated and for whomthe cause of death was known is shown in Figure 2. Among the37 patients excluded from the analysis of the outcomes of chemotherapy,10 (27 percent) died of tuberculosis and 7 (19 percent) diedof other causes during the follow-up period. Thus, a total of63 of the 171 patients died.
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.
Successful treatment was indicated by consistently negative sputum cultures for three consecutive months, and relapse by the resumption of shedding of tubercle bacilli; patients with relapses are included among those with successful treatment. Treatment failure was indicated by an inadequate response to at least three months of therapy. The events represented are deaths due to tuberculosis.
Factors Influencing Outcome
In univariate analyses, four factors were associated with thefailure of drug therapy to sterilize sputum cultures: previousadministration of more drugs, regimens including fewer previouslyunused drugs, in vitro resistance to more drugs, and male sex(this factor was marginally associated with failure) (Table 3).When all the factors were included in a multivariate model,only sex (odds ratio, 2.5; 95 percent confidence interval, 1.1to 6.2) and the number of drugs received previously (odds ratio,4.0; 95 percent confidence interval, 1.6 to 9.9) were significantlyassociated with treatment failure (P<0.03 and P<0.001,respectively).
Table 3. Predictors of Outcome of Chemotherapy in 134 Patients with Pulmonary Tuberculosis Resistant to Isoniazid and Rifampin.
Many regimens were employed. The most frequently used regimensconsisted of combinations of pyrazinamide, ethionamide, cycloserine,and aminosalicylic acid with one of the injectable aminoglycosideor polypeptide antimicrobial agents. Because of the small numbersof patients in each group, the efficacy of individual regimenscould not be analyzed.
Discussion
Treatment of patients with pulmonary tuberculosis due to M.tuberculosis resistant to rifampin, isoniazid, and other medicationsis complicated, risky, and of limited efficacy. Fully 46 percentof our patients with treatment failure or relapses died. Physiciansand society must recognize that multidrug-resistant tuberculosisis an ominous, deadly disease.
Patients who are treated unsuccessfully but remain alive posea major public health problem. They must be isolated becauseof the risk of transmitting virtually untreatable drug-resistantdisease. Drug-resistant tubercle bacilli were once believedless likely to be spread to contacts because the virulence ofthese organisms was diminished. However, a recent report20 demonstratedthat rates of infection (as detected with the tuberculin skintest) among contacts of patients with drug-resistant tuberculosiswere comparable overall to those among susceptible persons.In fact, because of their prolonged shedding of tubercle bacilli,previously treated patients with drug resistance had highernumbers of tuberculin-positive contacts than patients withoutresistance. Epidemics have been reported in which disease, includingfatal meningitis and highly destructive lung disease, has evolvedamong persons infected with these drug-resistant microbes13,14,15,21,22,23.Quarantine of patients with treatment failure in their homesis a potential remedy but is seldom achievable. Confinementof patients may protect others, but they must then bear theadditional burdens of isolation and stigmatization.
Because the number of drugs available was limited, our regimensfor retreatment frequently entailed the use of agents knownto be toxic or difficult to tolerate. When side effects occurredthat were not potentially life-threatening and substitutionof another medication was not feasible, we made great effortsto coach the patient through the drug intolerance, using bothsymptomatic palliation and psychological support. This requiredfamiliarity with each of the medications, as well as a greatdeal of time in giving care. Nonetheless, our success rate (65percent) in treating disease due to multidrug-resistant isolateswas less favorable than the rates in some earlier series ofpatients given retreatment in the pre-rifampin era24,25,26.The poorer results in the current study may be due to the largernumber of drugs to which the isolates from our patients wereresistant.
In our study an unsuccessful response to the therapy prescribedwas strongly associated with a greater number of drugs receivedpreviously and with male sex. The reason for the associationwith male sex is not readily apparent, but it may be relatedto behavioral as well as biologic factors. The association withprevious treatment with a greater number of drugs emphasizesthe importance of thoroughly studying the patient's treatmenthistory. Suboptimal previous therapy leads to the developmentof in vitro resistance. Thus, if the patient has already receiveda large number of drugs, few agents will still be availableto which the isolate will be susceptible, and the chances forsuccessful outcome decline.
However, some patients received drugs to which their organismswere susceptible according to conventional testing, yet theydid not respond clinically. This suggests that improved methodsof susceptibility testing are needed to provide more usefullaboratory guidelines for retreatment regimens. We are currentlyexploring the use of the rapid radiometric system (Bactec) todetermine minimal inhibitory concentrations27,28 -- values thatwe anticipate will replace the traditional "critical concentration"determined in solid agar.
Surgical resection as an adjunct to antituberculosis therapywas performed in patients who had amenable lesions and who werebeing treated with medical regimens deemed unlikely to effectpermanent control of their disease. We attempted to schedulesurgery so that it could be performed when the mycobacterialcount in sputum reached its expected nadir. Three patients withindeterminate responses to medical therapy and two without bacteriologicresponses to chemotherapy were clearly helped by resection.In the other two patients, whose sputum cultures had alreadybecome negative, the benefit of surgery was less clear.
When rifampin was introduced in 1971, it represented a majoradvance in antituberculosis treatment, leading to both short-coursechemotherapy1 and highly effective, well-tolerated managementof tuberculosis due to isoniazid-resistant organisms10. However,as anticipated,29 resistance to rifampin has emerged in substantialnumbers of patients, frequently in association with the previoususe of rifampin in an inadequate regimen and with noncompliance.Noncompliance contributed to the development of resistance torifampin in 74 of our patients (43 percent of this series of171 patients), and was suspected in many more. Noncompliancewith prescribed treatment is extremely common30. The most effectivesafeguard is the directly observed administration of medications.The treatment of patients with multidrug-resistant tuberculosisentails five to seven visits per week. The cost of retreatmentof patients in whom treatment fails and resistance to rifampinemerges should be considered when the economics of a tuberculosis-controlprogram are being evaluated31. Our very limited rates of successin treating multidrug-resistant disease raise serious concernsabout the future of tuberculosis control. If we, with all ourresources, can successfully treat less than 60 percent of suchpatients, what will happen in less ideal circumstances? To avoidsquandering the potential effectiveness of rifampin becauseof noncompliance or inept prescribing, systematic efforts arerequired to preserve the potency of this crucial drug againsttuberculosis.
This report includes patients first seen between 1973 and 1983.Thus, it is likely that few, if any, of these patients wereinfected with HIV. However, many patients who have contractedmultidrug-resistant tuberculosis have HIV infection14,15; theirresponse to treatment appears to be very poor, with high ratesof treatment failure and mortality32. Their response to antituberculosistherapy may be suboptimal, even when the organisms are susceptibleto the drugs used33,34. Thus, although we recommend similarstrategies for the therapy of drug-resistant tuberculosis whetheror not it accompanies HIV infection, the efficacy of such therapyin patients with HIV remains to be determined. New antimycobacterialagents are urgently needed to expand our therapeutic optionsfor multidrug-resistant tuberculosis.
Supported in part by a grant from the American Lung Associationof 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 computerand statistical assistance; to Barry Silverstein for graphics;and to LaJuana Simms, Kitty Gentry, Corine Eckman, and SharonForsberg 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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Multidrug-Resistant Tuberculosis
Iseman M. D., Goble M., Corrêa da Silva L. C., Corrêa da Silva L. M., Di Perri G., Vento S., Concia E., Cazzadori A., Telzak E. E., Sepkowitz K., Turett G.
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Antituberculosis-Drug Resistance
Chan-Tack K. M., Diaz J. F., Geerligs W. A., van Altena R., van der Werf T. S., Pablos-Méndez A., Raviglione M. C., Nunn P.
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N Engl J Med 1998;
339:1079-1080, Oct 8, 1998.
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