INT J TUBERC LUNG DIS 9(2):164–169
© 2005 IUATLD
Treatment outcome of multidrug-resistant tuberculosis
among Vietnamese immigrants
H. A. Ward,* D. D. Marciniuk,* V. H. Hoeppner,* W. Jones†
* Department of Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada; † International Organization
for Migration, Ho Chi Minh City, Vietnam
SUMMARY
OBJECTIVE:
To review the outcome for MDR-TB treatment among potential migrants from Vietnam.
S E T T I N G : All cases of documented MDR-TB treated by
the International Organization of Migration (IOM) in
Vietnam from 1989 to 2000 were reviewed.
M E T H O D S : MDR-TB was defined as isoniazid- and
rifampicin-resistant Mycobacterium tuberculosis. All
cases of TB treated by the IOM and recorded in the computerised database were reviewed to identify MDR-TB
cases. Demographics, chest radiograph results, drug resistance, drug use and dosage, duration of treatment,
and outcome were analysed.
R E S U L T S : Forty-four cases of MDR-TB were identified.
Treatment consisted of ambulatory directly observed
treatment with an 8-drug protocol: isoniazid, rifampi-
cin, pyrazinamide, ethambutol, capreomycin, ethionamide, ofloxacin and cycloserine. This initial protocol
was modified due to drug availability or drug intolerance. Patients were treated with a median of 8 drugs
(range 6–12). Mean duration of treatment for MDR-TB
was 23.0 (SD 11.4) months. Thirty-eight (86%) patients were cured and emigrated, one failed treatment
(2%), three were lost to follow-up (7%) and two died
(4%).
C O N C L U S I O N : Treatment for MDR-TB provided by the
IOM was effective in preparing a low-income population for migration.
K E Y W O R D S : multidrug resistant tuberculosis; treatment outcome; migration
TREATMENT OUTCOMES for multidrug-resistant
tuberculosis (MDR-TB, defined as resistance to at
least isoniazid [INH] and rifampicin [RMP]) vary between studies, with cure rates ranging from less than
40% to more than 80%.1–13 MDR-TB treatment programmes in these studies were based in countries with
variable resources, drug regimens, duration of treatment and drug delivery.
The optimal treatment of tuberculosis is the DOTS
strategy, based on World Health Organization (WHO)
guidelines to achieve cure rates of 85% and to prevent drug-resistant cases, particularly MDR-TB.14 Inadequate resources to provide the standard of treatment may contribute to an increasing prevalence of
MDR-TB in developing countries.15–17 From 1994 to
1997, the prevalence of primary MDR-TB in Vietnam
was 2.3% and resistance to one or more drugs was
32.5%.18 Among smear-positive cases who failed
treatment provided by the Vietnamese National TB
Programme (NTP), 47% had primary MDR-TB.19
Treatment for drug-resistant TB is virtually non-existent
in many developing countries.11
The International Organization for Migration (IOM)
is an international intergovernmental organisation
established in 1951 to ‘assist with the challenges of
migration’.20 IOM screens for pulmonary TB (PTB)
among migrants, supervises directly observed treatment (DOT) and defines cure in accordance with the
national guidelines of receiving countries. From 1975
to 1996, the IOM screened an estimated 1.5 million
Vietnamese migrants for TB.21 A computerised database has been maintained by the IOM of all Vietnamese emigrants treated for TB since 1989.
The objective of the present study was to review
treatment and outcomes prior to immigration of an
ambulatory MDR-TB treatment programme supervised by the IOM in Vietnam, a low-income country.
METHODS
This study was a retrospective review of all potential
migrants treated for MDR-TB by the IOM, Ho Chi
Minh City (HCMC), Vietnam, from 1 January 1989
to 30 June 2000. To be included for review, patients
Correspondence to: Heather A Ward, Department of Medicine, University of Saskatchewan, Box 109 Royal University Hospital, Saskatoon, Saskatchewan S7N 0W0, Canada. Tel: (1) 306-966-2180. Fax: (1) 306-966-1943. e-mail: heather.
[email protected]
Article submitted 5 March 2004. Final version accepted 10 June 2004.
Outcome of MDR-TB
required culture and drug susceptibility testing (DST)
with MDR-TB. All data were provided by the IOM.
The initial diagnosis of TB was made either by positive sputum smear and/or culture or progressive chest
radiograph changes. The standard regimen without
DST was directly observed 6-month treatment with
INH, RMP, pyrazinamide (PZA), and ethambutol
(EMB). All patients had PTB. Patients whose sputum
smears remained positive following a minimum of 5
consecutive months of standard treatment provided
by the IOM were considered at high risk for drug resistance. As culture and DST were not consistently available to the IOM, treatment with the 8-drug protocol
was initiated for all patients defined as high risk for
drug-resistant tuberculosis if they could provide payment for medications ($4000 US). Refugees’ treatment costs were covered by the receiving countries.
Cultures were processed at the Institute Pasteur,
HCMC. DST was completed by the NTP at Pham Ngoc
Thach Lung and Tuberculosis Hospital in HCMC,
using the direct proportion method with dilutions of
culture inoculated onto Löwenstein-Jensen (LJ) media.
At minimum, DST against INH, RMP and EMB was
available, and at most against INH, RMP, PZA, EMB,
ofloxacin (OFX), cycloserine (CS), rifabutin (RBT),
ethionamide (ETH), capreomycin (CM), and streptomycin (SM). DST against PZA was recognised to be
unreliable. Careful attention was paid to the pH of LJ
media for PZA testing (pH 5.5). Quality assurance
standards for the laboratories conducting smear testing and initial culture testing at Institute Pasteur were
monitored by the US Centers for Disease Control, Atlanta, GA (CDC)/IOM Laboratory Services. Quality
assurance for DST at the Vietnam NTP reference hospital, Pham Ngoc Thach, was performed by the International Union Against Tuberculosis and Lung Disease
(W Jones, personal communication).
Treatment for MDR-TB was started with an 8drug protocol utilised by the IOM. This included CM,
ETH, OFX and CS in addition to INH, RMP, PZA
and EMB. INH, RMP, PZA and EMB were continued
in the 8-drug protocol whether or not DST showed
resistance to any of the drugs because of the insufficient data on treatment of drug-resistant tuberculosis
when the programme was initiated, and the requirement by receiving countries for a conservative approach to treatment that included INH, RMP, PZA
(and EMB). As DST was not consistently available at
the NTP reference hospital, some patients defined as
high risk for drug-resistant tuberculosis and who
were receiving the 8-drug protocol never had culture
and DST completed. Results in those patients included in this study in whom culture and DST were
completed were often not available until many months
of treatment had been taken. DST results were used to
determine treatment if drug intolerance was present
and modification of the 8-drug protocol to an individually tailored regimen (ITR) was required. Other drugs,
165
including CS, kanamycin, amoxycillin/clavulinic acid,
and rifabutin were added to the regimen at the discretion of the treating physicians. Amikacin was substituted for CM and prothionamide for ETH depending
on drug availability during the study period.
Ambulatory DOT was provided at three locations
in HCMC. Injected medications were provided five
times a week for the first 2 months, then twice weekly
until treatment was completed. Oral medication was
directly observed 6 days per week and self-administered
on Sundays. Sputum smears were obtained every 2
weeks throughout the entire course of treatment.
Additional information in the computerised database included age, sex, weight, height, chest radiograph findings at initiation of treatment, sputum smear
results, sputum cultures, all medications and their
dosages, and outcome. While specific side effects were
not recorded in the database, the need to interrupt or
change medications due to side effects was recorded.
Previous treatment was self-reported.
Outcomes were cure, treatment failure, loss to
follow-up and death. Cure, which permitted emigration to the receiving country, was defined as 15 consecutive months of smear-negative sputum (18 consecutive months after 1999). End of treatment cultures
were not consistently available and were not used to
define cure. As cultures and DST availability were limited, treatment failure was determined by the treating
physicians and was based on symptoms, sputum smears
and chest radiograph response to treatment. Those
who did not complete treatment with the IOM were
defined as lost to follow-up. Home visits and counselling by the IOM treatment nurse were provided for
patients who did not report for DOT for one week.
Cause of death was not identified in the database.
Mean and standard deviation (SD) were calculated for continuous variables age and weight. Frequencies of drug resistance and median resistance to
number of drugs and median drug dosages were determined. 2 calculations for method of delivery and
loss to follow-up were calculated. Statistical analysis
was completed using SPSS (version 11.0, SPSS Inc,
Chicago, IL, USA).
RESULTS
Between January 1989 and June 2000, 2391 cases of
PTB were entered into the IOM database, of whom
135 received the 8-drug protocol. Cultures and DST
were available for 55 of these patients: 44 were identified with MDR-TB, seven had organisms susceptible
to either INH or RMP, and four grew atypical mycobacteria. No patients were reported to be human
immunodeficiency virus (HIV) positive. All patients
had PTB.
The mean age of the 44 patients with MDR-TB
was 48.8 (SD 17.3) years; 26 (59%) were male and
18 (41%) were female (Table 1); 32 (73%) patients
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The International Journal of Tuberculosis and Lung Disease
Table 1 Demographic characteristics of Vietnamese
immigrants with MDR-TB
Characteristic
Age (mean SD)
Sex
Male
Female
Destination
USA
Canada
Australia
Previous treatment
Cavity on initial chest radiograph
Weight kg (mean SD)
Number of patients
n 44
n (%)
48.8 years (17.3)
26 (59)
18 (41)
38 (86)
5 (11)
1 (2)
34 (77)
32 (73)
42.4 (7.8)
MDR-TB multidrug-resistant tuberculosis; SD standard deviation.
had a cavity on the initial chest radiograph, and 34
(77%) reported previous treatment.
Patients were resistant to a median of 4.5 drugs
(range 2–7) (Table 2): 13 were resistant to INH, RMP,
PZA and EMB, five to INH, RMP and PZA, 13 to
INH, RMP and EMB, and 13 to INH and RMP. In addition to INH and RMP resistance, 26/44 (59%) were
resistant to EMB, 18/37 (49%) to PZA, 31/38 (82%)
to SM, 21/37 (57%) to RBT, 16/40 (40%) to ETH, 1/38
(3%) to CS, and none to CM or OFX (Figure).
Patients with MDR-TB were treated with a median
of eight drugs (range 6–12) and were sensitive to a
median of five drugs (range 0–7). The median dose of
medications used is outlined in Table 3.
The median duration of the 8-drug protocol was
30.0 (range 8–72) months. Only four patients received
the 8-drug protocol for the entire course of treatment.
Of these, three had no side effects and one required
treatment to be temporarily interrupted. The remaining patients received ITRs determined by drug intolerance, DST, drug availability and the clinical discretion of the attending physician. No particular pattern
of drugs used in the ITRs was identified. Thirty-eight
patients were treated with ETH despite the resistance
of 40%, and only two were treated with clofazimine.
Thirteen had no side effects, 19 had side effects requiring a change in treatment and nine had medications interrupted. The medications most commonly
identified as causing side effects were EMB (34%),
Table 2
MDR-TB drug resistance and duration of treatment
Resistance
Drug resistance
Drug susceptibility
Susceptible to and used for treatment
Treatment
Months to conversion
Months 8-drug protocol and ITR
Median (range)
4.5 (2–7)
5 (0–7)
4 (0–7)
14.8 (6.0–51.0)
30.0 (8.0–72.0)
MDR-TB multidrug-resistant tuberculosis; ITR individually tailored regimen.
Figure
Frequency of drug resistance.
RMP (32%), INH (27%), and PZA (25%). ETH was
the second-line drug identified as most frequently
causing side effects (23%).
Of the 44 patients who began treatment for MDRTB, 38 (86%) completed treatment, met the definition of cure and emigrated; one patient failed treatment (2%), three were lost to follow-up (7%) and
two patients died (5%) (Table 2). For those who were
cured, all had 2-weekly sputum smears that were negative for the required period of time (15 months before to 1999, 18 months after 1999). End of treatment culture and DST were available for 21 of these
patients who were defined as cured based on sputum
smear results. All were culture-negative at the end of
treatment.
The three patients who were resistant to seven
drugs received an average of 40 months of treatment
and all were cured. One patient had treatment interrupted and modified because of side effects. This
patient was treated with three medications to which
susceptibility was demonstrated—RBT, OFX and
kanamycin. Two patients were treated with three
medications with demonstrated susceptibility—OFX,
CS and CM. Among the three patients who did not
return for treatment, the reason for loss to follow-up
Table 3
Median drug dosage used during MDR-TB treatment
Drug
Isoniazid
Rifampicin
Pyrazinamide
Ethambutol
Capreomycin
Cycloserine
Ethionamide
Ofloxacin
Rifabutin
Median dose
mg (range)
Median dose
mg/kg (range)
300 (0)
450 (300–600)
1250 (500–1750)
800 (400–1200)
750 (500–1000)
500 (250–750)
500 (500–1000)
500 (400–750)
300 (150–300)
7 (5–13)
7 (3–11)
31 (14–36)
17 (14–25)
19 (13–27)
14 (7–19)
16 (10–22)
13 (10–15)
7 (3–7)
MDR-TB multidrug-resistant tuberculosis.
Outcome of MDR-TB
was not defined in the database. The one patient who
was defined as a treatment failure had a positive culture at the end of treatment. DST in this patient demonstrated resistance to four drugs. Of the two patients who died, one was receiving treatment at the
time of death. This patient was resistant to five drugs.
The second patient who died was a no show for treatment for 9 months before being entered in the database as deceased. Resistance patterns were not unique
to patients who failed treatment or died.
DISCUSSION
The IOM treatment programme in Vietnam was an
ambulatory DOT programme without hospitalisation or surgical intervention. A standardised 8-drug
protocol, including INH, RMP, PZA and EMB was
initiated despite documented in vitro resistance to at
least INH and RMP. Treatment was completed with
an ITR in 38 of 44 patients with MDR-TB. All patients received a median of eight drugs.
Patients were strongly motivated to complete treatment because emigration was not permitted until the
receiving country’s definition of cure had been met.
This was probably one explanation as to why all but
three of the surviving patients completed a mean duration of 23 months of treatment with a median number of eight drugs. One patient failed treatment and
two died; 38 of 44 (86%) met the definition of cure.
Another possible explanation for the number of
patients who completed treatment was DOT. In this
ambulatory programme, doses were directly observed
in the IOM clinic. When patients missed more than
one week of treatment, the IOM treatment nurses
combined counselling with home visits. ‘DOT clearly
improves adherence in patients with tuberculosis.’22
DOT has been part of the TB treatment programme
in Denver, CO, since 1961 and part of the WHO TB
elimination programme since 1994.23,24 Denver consistently achieved about 95% completion rates with
DOT.25 In a review of the literature from 1966 to
1996, Chaulk and Kazandjian found that patients with
Table 4
167
DOT were more likely to complete treatment compared
to patients with self-administered treatment (SAT).26
The observed outcome of MDR-TB treatment in Vietnam was consistent with these reports.
We combined reports of outcome with DOT (11 and
current study) and compared them with four reports
of outcomes with SAT (Table 4).1,8,10,13 With data
from the reports, we compared patients who were
lost before completion of treatment as a per cent of
total patients. Eight of 101 patients who received
DOT were lost compared to 247 of 1217 patients
with SAT. A significantly higher number of patients
were lost before completion of treatment with SAT
(P 0.001). These data support the WHO recommendation of DOT in patients with MDR-TB.27
A review of previous reports describing treatment
and outcomes for MDR-TB revealed many differences.1,4–11,13 Previous treatment history, number of
drugs to which organisms were resistant, number
of drugs for treating MDR-TB and duration of treatment all varied. There were differences in patient demographics. Provision of surgical treatment differed
and medical treatment was provided in hospital or
ambulatory settings. Because of the unique characteristics of patients with MDR-TB, ITRs were provided.
No standard patient population, treatment regimens
or definition of cure were utilised, making comparisons difficult.
Eleven studies, including IOM Vietnam, were reviewed (Table 4). Two of these studies identified HIVpositive patients in their treatment group (52%5 and
16%8 of patients). Medications were selected either
by documented in vitro susceptibility and/or medications not previously used for treatment. In one study,
treatment was not initiated until DST was available.13
The median number of medications from all the
studies ranged from 2.5 to 6.1,4,6,9–11,13 Four of the 11
studies used a median of six or more drugs. Four
studies reviewed drug doses.1,6,10,13 INH and RMP
doses were identical in all studies. EMB, OFX, CS and
RBT doses were similar in all of the studies, but PZA
doses ranged from 20 to 30 mg/kg7 to 35 mg/kg.4,8
Literature review for MDR-TB treatment
Reference
Patients (n)
Resistance, median no. drugs
Treatment
Setting
Mode
Median no. of drugs
Duration (months)
Failed
Lost
Cured (%)
4
7
5
1
171
6
25
4
52
NR
105
4.2
8
9
6
10
13
11
Current
study
51
3
44
5
158
4.4
1011
3.7
50
2.5
66
6
44
4.5
Hosp
Hosp
Hosp
Hosp
Hosp
Hosp
Hosp
Hosp
Hosp
Amb
Amb
Amb
Amb
Amb
Amb
Amb
Amb
Amb Amb
DOT/NR
NR
NR
SAT
SAT
SAT
NR
SAT
SAT
DOT
4
NR
NR
5
1.6
6
5.7
5.3
6
6
24
15
18
24
8.2
20
21
23
12
23
47
8
NR
11
NR
NR
13
82
2
1
22
0
5
20
16
NR
17
192
19
5
56
64
56
50
65
75
77
48
62
83
Amb
DOT
8
23.0
1
3
86
MDR-TB multidrug-resistant tuberculosis; hosp hospitalisation; amb ambulatory; DOT directly observed treatment; NR not recorded; SAT selfadministered treatment.
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The International Journal of Tuberculosis and Lung Disease
Nine treatment programmes included hospitalisation1,4,5,7–10,13 and two programmes provided only
ambulatory treatment (11, current study). In six studies,
5% to 23% of patients underwent surgical treatment.1,4–7,9 Five treatment programmes utilised SAT
after hospitalisation.1,8–10,13 Two programmes provided
ambulatory treatment by DOT (11, current study).
Cure rates recorded in the programmes reviewed
ranged from 48% to 86%. In programmes with documented SAT, cure rates ranged from 50% to 75%.
Although patient numbers were small, outcomes of
more than 80% were documented only in the two
DOT programmes. These two programmes, in Vietnam and Peru, provided ambulatory treatment with no
hospital admissions and no surgery (11, current study).
Treatment programmes in Peru and Vietnam differed from other MDR-TB treatment programmes in
the use of DOT for all medication delivery. Only five
patients in Peru and three in Vietnam were lost to
follow-up despite the use of a median number of six
drugs in Peru and eight in Vietnam. This represented
the upper range of the median number of drugs used
for all treatment programmes. The median duration
of treatment was 23 months for both treatment programmes. This was again at the upper end of the
range of treatment duration for all reviewed programmes (range 8.2–24 months, Table 4). Medication doses in Vietnam were similar to those used in
other studies.1,6,10,13 DOT has been documented to
improve treatment adherence in tuberculosis and this
applied to MDR-TB treatment in both Vietnam and
Peru.22,25,26 Outcomes in Peru were ascribed to several factors by the authors, including the use of DOT,
low default rates, prolonged duration of treatment
and higher drug dosages.11 Similar programme features, including the use of DOT, were factors in the
86% cure rate documented by the IOM in Vietnam.
Outcomes in Peru and Vietnam suggest that the
use of DOT with an ambulatory care programme in a
resource-poor setting can provide successful treatment for MDR-TB. Prolonged treatment duration,
adherence to the treatment programme (DOT), and
number of drugs used may all have contributed to the
successful outcome for the ambulatory treatment programme in Vietnam.
CONCLUSION
Unique features of this ambulatory treatment programme of MDR-TB that resulted in a good outcome
include prolonged duration of treatment, adequate
drug dosages, directly observed treatment, and use of
multiple drugs (median 8) despite documented laboratory resistance. The incentive of migration once
treatment was successfully completed encouraged adherence to treatment. Although emphasis on preventing MDR-TB by the use of DOTS needs to be continued in developing countries, resources for treating
MDR-TB with successful programmes in the countries of origin need to be made available. It has been
demonstrated by the IOM in Ho Chi Minh City, Vietnam, that highly successful MDR-TB treatment programmes can be implemented. Further financial and
political commitment on behalf of the nations of immigration would allow these programmes to be instituted and reduce the incidence of MDR-TB in those
countries and in the migrants’ countries of origin.
Acknowledgements
All data was provided by the International Organization for
Migration (IOM), Ho Chi Minh City, Vietnam.
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RÉSUMÉ
O B J E C T I F : Revoir les résultats du traitement de la TBMR parmi des migrants potentiels venant du Vietnam.
C O N T E X T E : On a passé en revue tous les cas documentés
comme TB-MR et traités par l’Organisation Internationale de la Migration (OIM) au Vietnam de 1989 à 2000.
M É T H O D E S : La TB-MR a été définie comme une résistance de Mycobacterium tuberculosis à l’isoniazide et à
la rifampicine. On a revu tous les cas de TB traités par
l’OIM et enregistrés dans la base de données informatiques en vue de l’identification des cas de TB-MR. Les caractéristiques démographiques, les résultats du cliché
thoracique, la résistance aux médicaments, l’utilisation
des médicaments et leur dosage, la durée du traitement
et ses résultats ont fait l’objet d’une analyse.
R É S U L T A T S : On a pu identifier 44 cas de TB-MR. Le
traitement avait consisté en une thérapie directement ob-
servée et ambulatoire avec un protocole comportant
huit médicaments : isoniazide, rifampicine, pyrazinamide,
éthambutol, capréomycine, éthionamide, ofloxacine et
cyclosérine. Ce protocole initial a été modifié en fonction de la disponibilité des médicaments ou de l’intolérance à leur égard. Les patients ont été traités avec un
nombre médian de huit médicaments (extrêmes 6 à 12).
La durée moyenne du traitement pour la TB-MR a été
de 23,0 (DS 11,4) mois. On a noté 86% de guérison avec
émigration, un échec (2%), trois pertes de vue (7%) et
deux décès (4%).
C O N C L U S I O N : Le traitement de la TB-MR par l’OIM a
été efficient pour préparer à l’émigration une population
à faibles ressources.
RESUMEN
O B J E T I V O : Evaluar el resultado del tratamiento de
tuberculosis con multidrogo-resistencia (TB-MDR) entre los candidatos a la emigración en Vietnam.
M A R C O D E R E F E R E N C I A : Se revisaron todos los casos
de tuberculosis con multidrogo-resistencia tratados por
la Organización Internacional para las Migraciones
(OIM) en Vietnam desde 1989 hasta 2000.
M É T O D O S : Se definió TB-MDR como aquella causada
una cepa de Mycobacterium tuberculosis resistente a
isoniacida y a rifampicina. Se revisaron todos los casos
de tuberculosis tratados por la OIM y registrados en una
base de datos informatizada, para identificar los casos
de TB-MDR. Se analizaron las características demográficas, los resultados de la radiografía de tórax, la sensibilidad a las drogas, los medicamentos y las dosis empleadas, la duración del tratamiento y los resultados.
Se identificaron 44 casos de TB-MDR.
El tratamiento fue ambulatorio directamente observado
siguiendo un protocolo con 8 medicamentos : isoniacida, rifampicina, piracinamida, etambutol, capreomicina, etionamida, ofloxacina y cicloserina. Este protocolo inicial se modificó según la disponibilidad o la
intolerabilidad a los medicamentos. Los pacientes recibieron tratamiento con un promedio de 8 medicamentos
(entre 6 y 12). La duración media del tratamiento de la
TB-MDR fue 23 meses (DS 11,4). Treinta y ocho
(86%) pacientes curaron y emigraron, un paciente presentó fracaso terapéutico (2%), tres (7%) se perdieron
durante el seguimiento y dos pacientes fallecieron (4%).
C O N C L U S I Ó N : El tratamiento de la TB-MDR, administrado por la OIM, fue eficaz para preparar una población de bajos ingresos para la emigración.
RESULTADOS :