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Bull World Health Organ 2015;93:125–130 |doi: http://dx.doi.org/10.2471/BLT.14.138560
Lessons from the field
125
Implementing rapid testing for tuberculosis in Mozambique
James Cowan,a
Cathy Michel,a
Ivan Manhiça,b
Claudio Monivo,a
Desiderio Saize,a
Jacob Creswell,c
Stephen Gloyda
& Mark Miceka
Introduction
People infected with human immunodeficiency virus (HIV)
are susceptible to tuberculosis. This has led to an HIV-driven
tuberculosis epidemic in sub-Saharan Africa over the past two
decades.1
Diagnosing tuberculosis is often difficult given the
low sensitivity of smear microscopy. Among people infected
with HIV, smear microscopy is even less sensitive due to the
lower bacterial load in co-infected individuals.2
Xpert® MTB/RIF (Xpert®; Cepheid, Sunnyvale, United
States of America) is a rapid and fully-automated molecular
test that uses real-time polymerase chain reaction on sputum
samples to simultaneously detect Mycobacterium tuberculosis
deoxyribonucleic acid and the genetic sequence indicative of
rifampicin resistance.3,4
The test has 88% sensitivity for tuber-
culosis and 94% sensitivity for rifampicin resistance. Given the
high sensitivity, the test is more effective than sputum smear
microscopy in diagnosing tuberculosis in HIV-infected people.
Therefore the World Health Organization (WHO) has recom-
mended the use of Xpert® for diagnosis of tuberculosis in coun-
tries with high prevalence of HIV infection and multi-drug
resistant tuberculosis (MDR-TB).5,6
The four-module Xpert®
machine and desktop computer retails for 17 000 United States
dollars (US$) in low-income countries and each cartridge (one
per sample) costs an additional US$ 10.7
This paper describes
the introduction of Xpert® in Mozambique.
Local setting
Mozambique has a high burden of tuberculosis. In 2012,
WHO estimated an incidence of 552 per 100 000 people,
which corresponds to approximately 140 000 new cases.
However, only 34% of these estimated cases are diagnosed
and notified to the national tuberculosis programme. Most,
(94%), new tuberculosis patients are tested for HIV8
and 58%
are found to be co-infected. Tuberculosis diagnosis is done in
people reporting a persistent cough, using smear microscopy
on sputum samples.8
MDR-TB testing is seldom done since
culture of M. tuberculosis is not routinely available.8
New cases
typically receive first-line therapy. The treatment success rate is
85% for new sputum smear-positive patients who start treat-
ment at a public treatment centre.9
First-line therapy typically
includes isoniazid, rifampicin, pyrazinamide and ethambutol.
Second-line therapy typically includes kanamycin, levofloxa-
cin, ethionamide, cycloserine, ethambutol and pyrazinamide.
In 2012, an estimated 3.5% (4900 people) of the new
estimated tuberculosis patients had MDR-TB; however, only
213 patients with MDR-TB started appropriate second-line
treatment.8
Both in Mozambique and globally, the prevalence
of MDR-TB tuberculosis is increasing. Therefore improved
MDR-TB diagnostics and access to treatment are priorities
for the Mozambican national tuberculosis programme and
the global health community.8
Planned intervention
To increase the number of people diagnosed and treated
with tuberculosis and to improve MDR-TB detection and
treatment, the Xpert® implementation project was approved
by the Mozambican Ministry of Health, with support from
Health Alliance International. We chose to use a two-step
testing algorithm for individuals suspected of having pulmo-
Problem In Mozambique, pulmonary tuberculosis is primarily diagnosed with sputum smear microscopy. However this method has low
sensitivity,especiallyinpeopleinfectedwithhumanimmunodeficiencyvirus(HIV).Patientsareseldomtestedfordrug-resistanttuberculosis.
Approach The national tuberculosis programme and Health Alliance International introduced rapid testing of smear-negative sputum
samples. Samples were tested using a polymerase-chain-reaction-based assay that detects Mycobacterium tuberculosis deoxyribonucleic
acid and a mutation indicating rifampicin resistance; Xpert® MTB/RIF (Xpert®). Four machines were deployed in four public hospitals along
with a sputum transportation system to transfer samples from selected health centres. Laboratory technicians were trained to operate the
machines and clinicians taught to interpret the results.
Local setting In 2012, Mozambique had an estimated 140 000 new tuberculosis cases, only 34% of which were diagnosed and treated. Of
tuberculosis patients, 58% are HIV-infected.
Relevant changes From 2012–2013, 1558 people were newly diagnosed with tuberculosis using sputum smears at intervention sites.
Xpert® detected M. tuberculosis in an additional 1081 sputum smear-negative individuals, an increase of 69%. Rifampicin resistance was
detected in 58/1081 (5%) of the samples. However, treatment was started in only 82% of patients diagnosed by microscopy and 67% of
patients diagnosed with the rapid test. Twelve of 16 Xpert® modules failed calibration within 15 months of implementation.
Lessons learnt Using rapid tests to diagnose tuberculosis is promising but logistically challenging. More affordable and durable platforms
areneeded.Allpatientsdiagnosedwithtuberculosisneedtostartandcompletetreatment,includingthosewhohavedrugresistantstrains.
a
Health Alliance International, 1107 NE 45th Street, Suite 350, Seattle, 98105, United States of America.
b
Mozambican National Tuberculosis Control Programme, Maputo, Mozambique.
c
Stop TB Partnership, World Health Organization, Geneva, Switzerland.
Correspondence to James Cowan (email: jcowan22@uw.edu).
(Submitted: 2 April 2014 – Revised version received: 8 November 2014 – Accepted: 11 November 2014 – Published online: 26 November 2014 )
Lessons from the field
Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560126
Lessons from the field
Rapid testing for tuberculosis, Mozambique James Cowan et al.
nary tuberculosis. All sputum samples
were analysed using smear microscopy
and new patients with at least one posi-
tive sputum smear out of two separate
samples were treated with first-line
tuberculosis therapy. Patients with two
separate smear negative results were
retested using Xpert® on one of the
original samples.
In the beginning of February 2012,
four Xpert® machines were deployed at
two district and two urban public hospi-
tals in four districts in Sofala and Manica
provinces. We developed a transporta-
tion network to transfer smear negative
sputum samples from three of the 10
surrounding health centres to the two
urban hospitals. Eight remote health
facilities routinely transferred samples
to the two district hospitals via exist-
ing sputum transport networks. This
covered approximately 5% of all sputum
samples tested in Mozambique.10
Initial training and technical sup-
port for clinicians and laboratory staff
in the four hospitals was led by Health
Alliance International. Prior to Xpert®
testing initiation, each site was given
a day-long training session to train
laboratory technicians to operate the
machines and teach clinicians to in-
terpret the results. Initial introductory
meetings were also held with district
and provincial ministry of health staff
and supervisors. Health Alliance In-
ternational trainers then provided at
least weekly supervision visits to each
site with focused training for techni-
cians with elevated testing error rates,
to troubleshoot problems, to review
cartridge procurement and distribution
and to undertake initial calibration. The
trainers also monitored the testing care
cascade to ensure that patients received
their test results and were linked to ap-
propriate treatment. Daily Xpert® testing
and long-term management – such as
technical support, cartridge procure-
ment and routine maintenance – was
assumed by the Ministry of Health after
appropriate training.
The national tuberculosis pro-
gramme registers new tuberculosis pa-
tients as either sputum smear negative or
positive. The system has no capacity to
record molecular test results. Therefore,
laboratories using the rapid tests were
instructed to report patients testing
positive with Xpert® as sputum smear
negative cases. However, this instruc-
tion was not always followed and an
estimated 5–10% of sputum smear nega-
tive cases that tested positive on Xpert®
were reported as sputum smear positive.
The performance of this project
was monitored from reports gener-
ated from individual Xpert® machines.
These reports were collected by hand
each month, and information extracted
included the number of tests run per
quarter, a summary of the results, and
lists of patients that tested positive,
which were reconciled with the tuber-
culosis treatment registries. This was
combined with quarterly data from the
national tuberculosis programme on
the reported number of sputum smears
analysed and the number of patients
started on tuberculosis treatment.
Xpert® was approved for general
use by the Mozambican Ministry of
Health and the national tuberculosis
programme formally approved the
implementation of this project. This
implementation project was not a formal
research study thus the University of
Washington institutional review board
declined to provide a full review of this
proposal.
Implementation and results
From 1 January 2012 to 31 December
2012; 1558/12 509 (12%) people tested
at the four hospitals had sputum smear
positive results. Of the 10 951 people
with sputum smear negative results,
8631 (79%) were tested using Xpert®
and 1081 (13%) were positive for tuber-
culosis. Thus, during this intervention
Xpert® testing increased the diagnosis
of bacteriologically-confirmed pulmo-
nary tuberculosis by 1081/1558 (69%).
Rifampicin resistance was detected in
58/1081 (5%) samples. Overall, 1019
(12%) of tests failed because of machine
errors, and invalid or no results due to
energy shortages.
We reviewed the records of 445
newly-diagnosed patients from the four
hospitals in the second quarter of 2012
and found that 26% [115/445] had not
been started on treatment (18% [35/200]
of those diagnosed by microscopy and
33% [80/245] diagnosed using Xpert®).
For patients with rifampicin resistance,
53% [31/58] were not started on second-
line treatment. Three patients with
rifampicin resistance were mistakenly
initially started on first-line treatment
but were converted to second-line
treatment.
During 2012, 5076 people were
placed on treatment in the four interven-
tion districts, an increase of 632 patients
(14.2%) over the baseline yearly aver-
age for these districts which was 4444
patients (15 554 patients were treated
in these districts during the 3.5 years
before implementation).
Challenges
Despite encouraging outcomes, there
were several programmatic and op-
erational challenges in implementing
and maintaining the Xpert® machines
(Table 1).
One computer failed within
six months, despite being attached to
a surge protector/current stabilizer.
Twelve of the original 16 (75%) Xpert®
modules broke or failed calibration
within 15 months and had to be re-
placed. In early 2013, Xpert® cartridges
and calibration kits were back-ordered,
resulting in several days without Xpert®
cartridges despite ample lead-time in
ordering.11
Updating antivirus software
and operating systems and transferring
data from the local computer to Cepheid
in California, USA, was also difficult.
Cepheid depends on Xpert® machines
being connected to the internet to be
able to diagnose problems remotely –
this was not feasible in Mozambique
and caused significant delays. Over time,
shipments of cartridges and customer
service improved as Cepheid employees
and our team learned how to work with
each other. However, importing con-
sumables to Mozambique and clearing
customs remained challenging, expen-
sive and time-consuming.
The lack of a notification system
to report positive Xpert® results to the
national tuberculosis programme and
no ability to automatically upload re-
sults electronically to a central secure
database made it challenging to assess
the impact of this intervention. It was
difficult to remotely monitor Xpert® test-
ing and notify key individuals in a timely
fashion – such as provincial MDR-TB
care coordinators when a patient tested
positive for rifampicin resistance. WHO
guidance on recording and reporting
test results should allow national tuber-
culosis programmes to better monitor
performance.12
The current two-step testing algo-
rithm likely caused delays in tuberculo-
sis diagnosis relative to using Xpert® as
a first-line test. Some patients returned
after 24 hours for their smear results,
but did not get their subsequent Xpert®
Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560 127
Lessons from the field
Rapid testing for tuberculosis, MozambiqueJames Cowan et al.
result. The need for repeat visits to
establish a diagnosis may have led to
higher pretreatment loss to follow-up.
In the beginning, sites did not routinely
collect patient contact information so it
was impossible to reach these primary
defaulters. Initially there was no proto-
col to routinely reconcile laboratory and
treatment registries to ensure that all pa-
tients diagnosed with tuberculosis were
started on treatment. Efforts are ongo-
ing to improve the entire tuberculosis
care cascade and to increase treatment
initiation rates.
Lessons learnt
Our small-scale implementation proj-
ect allowed us to gain important prac-
tical experience about the strengths
and limitations of this new diagnostic
technique (Box 1). Rapid tests have the
potential to improve the diagnosis of
tuberculosis and identify drug resis-
tance. However, the tools are expensive
and we experienced problems with
the machines, data transfer, linkage
to tuberculosis treatment initiation,
reporting and follow-up. If the use of
rapid diagnostic tests for tuberculosis is
expanded to the national level, system
improvements are needed to prevent
these problems from occurring at a
larger scale.
The national tuberculosis pro-
gramme is committed to effective care
of all tuberculosis patients in Mozam-
bique. Improving diagnosis is a part of
this commitment and, therefore, rapid
tests like Xpert® will be provided to
more health centres. However, afford-
able and durable tuberculosis diag-
nostic platforms that can handle the
stresses of laboratory environments in
low-resource settings are still needed.
Table 1.	 Responses to technical and logistical challenges encountered when implementing rapid tests for tuberculosis, Mozambique
2012–2013
Challenge Reason Response
High testing error rates Laboratory technicians unfamiliar with
Xpert®
Targeted training of technicians at facilities with high error rates.
Error rate decreased from 12% in first year to 6% in the second year
Higher (20%) cartridge error rates
when cartridges were stored in non-air
conditioned rooms
Installed air conditioners in cartridge storage areas
Loss to follow-up Laboratory registries were not routinely
reconciled with tuberculosis treatment
registries
Developed monthly meetings to reconcile laboratory and treatment
registries
Current two-step testing algorithm
for tuberculosis delays patient results,
decreasing the percentage of patients
started on tuberculosis treatment
Ensured that laboratories collect patient addresses and phone
numbers
Used existing community health workers to find and treat defaulters
Start using Xpert® as a first-line test for high risk patients (those with
HIV infection, diabetes, cancer, children) and those at risk for MDR-TB
Loss to follow-up for patients
with rifampicin resistance
Some technicians did not initially
understand that Xpert® tested for
tuberculosis and rifampicin resistance
Additional staff education
Pilot a remote monitoring system to immediately notify key
individuals by SMS when a patient tests positive for rifampicin
resistance
Lack of real-time monitoring
and evaluation
Xpert® originally designed to transmit
data via Ethernet cables, not cell phone-
based data connections that are widely
available in low-income countries
Ministry of Health and national tuberculosis programme reporting
systems need to be adapted to incorporate test results
Limited ability to access test results and
aggregate these by district, province or
national level
Pilot a remote monitoring system for Xpert® that automatically
transmits test results to a central database
Determining an appropriate
testing algorithm
Balancing the high cost of Xpert® with
increased sensitivity for detecting
tuberculosis and rifampicin resistance
Start using Xpert® as a first-line test for high risk patients (those with
HIV infection, diabetes, cancer, children) and those at risk for MDR-TB
Xpert® durability Poor understanding of routine
maintenance requirements in dusty,
non-temperature controlled remote
laboratories
Use Xpert® at health centres with adequate staff and maintenance
support
Develop maintenance protocols specific to remote laboratories in
Mozambique
Lusophone staff struggling
with English software
Software was initially only available in
English
A new version was released that supports several languages,
including Portuguese
HIV: human immunodeficiency virus; MDR-TB: multi-drug resistant tuberculosis; SMS: short message service.
Box 1.	Summary of main lessons learnt
•	 Xpert® MTB/RIF (Xpert®) testing increased the number of confirmed bacteriologically
positive tuberculosis cases. However, one third of patients diagnosed by Xpert® did not
receivetuberculosistreatment,highlightingtheneedtostrengthentheoveralltuberculosis
care cascade.
•	 ImplementationandmaintenanceofXpert®machinesarecostlyandlogisticallychallenging,
which creates a need for more affordable and durable molecular testing platforms.
•	 Of the tuberculosis patients diagnosed with Xpert®, 5% were resistant to rifampicin,
highlighting the need to develop a multi-drug resistance tuberculosis programme in
Mozambique.
Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560128
Lessons from the field
Rapid testing for tuberculosis, Mozambique James Cowan et al.
‫ملخص‬
‫موزامبيق‬ ‫يف‬ ‫للسل‬ ‫الرسيع‬ ‫االختبار‬ ‫تنفيذ‬
‫رئييس‬ ‫بشكل‬ ،‫موزامبيق‬ ‫يف‬ ،‫الرئوي‬ ‫السل‬ ‫تشخيص‬ ‫يتم‬ ‫املشكلة‬
‫هذا‬ ‫ولكن‬ .‫البلغم‬ ‫لطاخة‬ ‫باستخدام‬ ‫املجهري‬ ‫الفحص‬ ‫طريق‬ ‫عن‬
‫األشخاص‬ ‫لدى‬ ‫سيام‬ ‫ال‬ ،‫منخفضة‬ ‫بحساسية‬ ‫يتمتع‬ ‫األسلوب‬
‫فحص‬ ‫يتم‬ ‫ما‬ ً‫ا‬‫ونادر‬ .‫البرشي‬ ‫املناعي‬ ‫العوز‬ ‫بفريوس‬ ‫املصابني‬
.‫لألدوية‬ ‫املقاوم‬ ‫بالسل‬ ‫اإلصابة‬ ‫لتحديد‬ ‫املرىض‬
‫الدويل‬ ‫والتحالف‬ ‫السل‬ ‫ملكافحة‬ ‫الوطني‬ ‫الربنامج‬ ‫قام‬ ‫األسلوب‬
.‫للطاخة‬ ‫اإلجيابية‬ ‫البلغم‬ ‫لعينات‬ ‫الرسيع‬ ‫االختبار‬ ‫بتنفيذ‬ ‫للصحة‬
‫البوليمرياز‬ ‫تفاعل‬ ‫عىل‬ ‫يستند‬ ‫اختبار‬ ‫باستخدام‬ ‫العينات‬ ‫اختبار‬ ‫وتم‬
‫الريبي‬ ‫واحلمض‬ ‫السلية‬ ‫املتفطرة‬ ‫البكرتيا‬ ‫يكشف‬ ‫الذي‬ ‫املتسلسل‬
‫إىل‬ ‫تشري‬ ‫التي‬ ‫الريفامبيسني‬ ‫ومقاومة‬ ‫األكسجني‬ ‫منزوع‬ ‫النووي‬
Xpert® MTB/RIF”“ ‫السل‬ ‫داء‬ ‫واختبار‬ ‫طفرة؛‬ ‫حدوث‬
‫عمومية‬ ‫مستشفيات‬ ‫أربعة‬ ‫يف‬ ‫أجهزة‬ ‫أربعة‬ ‫نرش‬ ‫وتم‬ .)®(Xpert
.‫املختارة‬ ‫الصحية‬ ‫املراكز‬ ‫من‬ ‫العينات‬ ‫لنقل‬ ‫البلغم‬ ‫نقل‬ ‫نظام‬ ‫مع‬
‫اخلرباء‬ ‫وتثقيف‬ ‫األجهزة‬ ‫تشغيل‬ ‫عىل‬ ‫املختربات‬ ‫فنيي‬ ‫تدريب‬ ‫وتم‬
.‫النتائج‬ ‫تفسري‬ ‫عىل‬ ‫الرسيريني‬
‫يف‬ ‫اجلديدة‬ ‫السل‬ ‫حاالت‬ ‫بلغت‬ ،2012 ‫عام‬ ‫يف‬ ‫املحلية‬ ‫املواقع‬
‫تشخيص‬ ‫يتم‬ ‫ومل‬ ،‫حالة‬ 140000 ‫التقديرات‬ ‫وفق‬ ‫موزامبيق‬
‫مرىض‬ ‫من‬ ‫املائة‬ ‫يف‬ ‫ستني‬ ‫نسبة‬ ‫وكانت‬ .‫منها‬ % 34 ‫سوى‬ ‫وعالج‬
.‫البرشي‬ ‫املناعي‬ ‫العوز‬ ‫بفريوس‬ ‫مصابة‬ ‫السل‬
‫تشخيص‬ ‫تم‬ 2013 ‫عام‬ ‫إىل‬ 2012 ‫عام‬ ‫من‬ ‫الصلة‬ ‫ذات‬ ‫ات‬ ّ‫ر‬‫التغي‬
‫يف‬ ‫البلغم‬ ‫لطاخات‬ ‫باستخدام‬ ‫بالسل‬ ً‫ا‬‫حديث‬ ً‫ا‬‫شخص‬ 1558 ‫إصابة‬
‫السلية‬ ‫املتفطرة‬ ‫البكرتيا‬ ®Xpert ‫اختبار‬ ‫وكشف‬ .‫التدخل‬ ‫مواقع‬
‫مقاومة‬ ‫كشف‬ ‫وتم‬ .% 69 ‫نسبتها‬ ‫بزيادة‬ ،‫إضافية‬ ‫عينة‬ 1081 ‫يف‬
‫تم‬ ،‫ذلك‬ ‫ومع‬ .‫العينة‬ ‫من‬ )% 5( 1081/58 ‫يف‬ ‫الريفامبيسني‬
‫عن‬ ‫تشخيصهم‬ ‫تم‬ ‫الذين‬ ‫املرىض‬ ‫من‬ ‫فقط‬ % 82 ‫يف‬ ‫العالج‬ ‫بدء‬
‫تشخيصهم‬ ‫تم‬ ‫الذين‬ ‫املرىض‬ ‫من‬ % 67‫و‬ ‫املجهري‬ ‫الفحص‬ ‫طريق‬
‫أصل‬ ‫من‬ ‫وحدة‬ ‫عرشة‬ ‫اثني‬ ‫وعجزت‬ .‫الرسيع‬ ‫االختبار‬ ‫باستخدام‬
ً‫ا‬‫شهر‬ 15 ‫غضون‬ ‫يف‬ ‫املعايرة‬ ‫عن‬ ®Xpert ‫الختبارات‬ ‫وحدة‬ 16
.‫التنفيذ‬ ‫من‬
‫تشخيص‬ ‫يف‬ ‫الرسيعة‬ ‫االختبارات‬ ‫استخدام‬ ‫املستفادة‬ ‫الدروس‬
.‫اللوجستية‬ ‫الناحية‬ ‫من‬ ‫حتديات‬ ‫عىل‬ ‫ينطوي‬ ‫ولكنه‬ ‫واعد‬ ‫أمر‬ ‫السل‬
‫وتتسم‬ ‫معقولة‬ ‫تكلفة‬ ‫ذات‬ ‫أكثر‬ ‫منصات‬ ‫إىل‬ ‫حاجة‬ ‫ثمة‬ ‫وتوجد‬
‫بالسل‬ ‫إصابتهم‬ ‫تشخيص‬ ‫يتم‬ ‫الذين‬ ‫املرىض‬ ‫مجيع‬ ‫وحيتاج‬ .‫بالقوة‬
‫بسالالت‬ ‫املصابني‬ ‫املرىض‬ ‫ذلك‬ ‫يف‬ ‫بام‬ ،‫وإمتامه‬ ‫العالج‬ ‫بدء‬ ‫إىل‬
.‫لألدوية‬ ‫مقاومة‬
摘要
莫桑比克实施结核病快速检测
问题 在莫桑比克,肺结核主要使用痰涂片镜检确诊。
然而,这种方法灵敏度较低,特别是在病人感染了艾
滋病病毒(HIV)的时候。患者很少接受耐药结核病
检测。
方法 国家结核病项目和国际健康联盟推出使用涂片
阴性痰标本的快速检测。样品使用以聚合酶链反应
为基础的化验进行检测,该化验为 Xpert®MTB/RIF
(Xpert®),可发现分枝杆菌肺结核脱氧核糖核酸和指
示利福平抗性的突变。在四所公立医院部署了四台机
器和痰运输系统,以从选定的医疗中心转送样本。培
训实验室技术人员来操作这些机器并指导临床医生解
释结果。
当地状况 2012年,莫桑比克估计有14万名新结核病例,
其中只有 34% 接受诊断和治疗。58% 的结核病患者感
染艾滋病毒。
相关变化 从 2012 至 2013 年,在干预点通过痰涂片诊
断 1558 例新确诊结核病患者。Xpert® 在额外 1081 个
样本中发现结核分枝杆菌,增加达 69%。在这 1081 例
样本中有 58 例(5%)发现利福平抗性。然而,显微
镜诊断的患者中只有 82% 开始接受治疗,快速检测诊
断的患者中只有 67% 开始接受治疗。在实施的 16 个
月中,15 个 Xpert® 模块中有 12 个没有校准。
经验教训 使用快速检测来诊断肺结核是有希望的,但
在逻辑上具有挑战性。需要更多实惠且耐用的平台。
所有确诊患有肺结核的患者需要开始接受并完成治
疗,包括那些带有耐药菌株的患者。
Résumé
Mise en œuvre d’un test de dépistage rapide de la tuberculose au Mozambique
Problème Au Mozambique, la tuberculose pulmonaire est
principalementdiagnostiquéeenexaminantdesfrottisd’expectoration
aumicroscope.Cependant,cetteméthodeestpeusensible,enparticulier
chezlespersonnesinfectéesparlevirusdel’immunodéficiencehumaine
(VIH). Les patients sont rarement testés pour la tuberculose résistante
aux médicaments.
Approche Le programme national de lutte contre la tuberculose et
Health Alliance International ont introduit le dépistage rapide sur les
échantillonsdefrottisd’expectorationnégatifs.Leséchantillonsontété
testésàl’aided’untestbasésurl’amplificationenchaîneparpolymérase,
qui détecte l’acide désoxyribonucléique de la bactérie Mycobacterium
tuberculosis et une mutation indiquant la résistance à la rifampicine:
Remote monitoring and evaluation of
rapid testing systems may improve with
the use of platforms such as GxAlert,
XpertSMS and the Cepheid cloud
system.13
Finally, while innovation in
diagnostic tests is important, this is
only one part of the tuberculosis care
cascade. When increasing the number
of people diagnosed with tuberculosis,
attention is needed to ensure they re-
ceive the appropriate treatment, care
and support. ■
Acknowledgement
Health Alliance International is a centre
within the Department of Global Health,
University of Washington, Seattle, USA.
Competing interests: None declared.
Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560 129
Lessons from the field
Rapid testing for tuberculosis, MozambiqueJames Cowan et al.
Xpert®MTB/RIF(Xpert®).Quatremachinesontétédéployéesdansquatre
hôpitauxpublicsavecunsystèmedetransportdesfrottisd’expectoration
pourtransférerleséchantillonsdepuislescentresdesantésélectionnés.
Les techniciens de laboratoire ont été formés à utiliser les machines et
les cliniciens ont appris à interpréter les résultats.
Environnement local En 2012, le nombre de nouveaux cas de
tuberculose au Mozambique était estimé à 140 000, dont seuls 34%
étaient diagnostiqués et traités. Des patients atteints de tuberculose,
58% étaient infectés par leVIH.
Changements significatifs Depuis 2012–2013, 1558 personnes ont
été nouvellement diagnostiquées comme tuberculeuses par examen
desfrottisd’expectorationdanslessitesd’intervention.Xpert®adétecté
M. tuberculosis dans 1081 échantillons supplémentaires, soit une
augmentation de 69%. La résistance à la rifampicine a été détectée
dans 58 des 1 081 échantillons (5%). Cependant, le traitement avait
commencé chez seulement 82% des patients diagnostiqués par
microscopieet67%despatientsdiagnostiquésparletestdedépistage
rapide.Parmiles16 modulesXpert®,12 d’entreeuxn’avaientpasréussi
l’étalonnage au cours des 15 mois de la mise en œuvre.
Leçons tirées L’utilisation de tests de dépistage rapide pour
diagnostiquer la tuberculose est prometteuse, mais reste difficile sur
le plan logistique. Des plateformes plus abordables et durables sont
nécessaires. Tous les patients diagnostiqués comme tuberculeux
doivent commencer et terminer leur traitement, y compris ceux avec
des souches résistantes aux médicaments.
Резюме
Применение метода экспресс-тестирования на туберкулез в Мозамбике
Проблема Диагностика туберкулеза легких в Мозамбике в
основном проводится методом микроскопии мазка мокроты.
Однако этот метод имеет низкую чувствительность, особенно
у людей, инфицированных вирусом иммунодефицита человека
(ВИЧ). Пациенты редко проверяются на наличие лекарственно-
устойчивого туберкулеза.
Подход Национальная программа борьбы с туберкулезом
и некоммерческая организация Health Alliance International
внедрили метод экспресс-тестирования мазков мокроты с
отрицательнымрезультатомпримикроскопии.Образцымокроты
проверялись путем анализа на основе полимеразной цепной
реакции,которыйопределяетналичиедезоксирибонуклеиновой
кислоты Mycobacterium tuberculosis и мутации, указывающие
на устойчивость к рифампицину. Данный экспресс-тест
называется Xpert® MTB/RIF (Xpert®). В четырех государственных
больницах были развернуты четыре установки и организована
транспортная система для передачи образцов мокроты из
избранных медицинских центров. Было проведено обучение
лаборантов работе на данных установках и обучение врачей
методу интерпретации результатов.
Местные условия Согласно оценкам, в 2012 году в Мозамбике
возникло примерно 140 000 новых случаев туберкулеза, лишь
34% из которых были диагностированы и вылечены. При этом
58% больных туберкулезом являются одновременно ВИЧ-
инфицированными.
Осуществленные перемены За период 2012-2013 гг. туберкулез
был диагностирован у 1558 человек по результатам анализов
мазков мокроты, проведенных в медицинских учреждениях.
При анализе по методу Xpert® были обнаружены микобактерии
в дополнительных 1081 образцах, что составляет увеличение на
69%.Устойчивостькрифампицинубылаобнаруженав58из1081
(5%) образцов.Однаколечениебылоначатотольковотношении
82%пациентовсдиагнозом,полученнымметодоммикроскопии,
и 67% пациентов с диагнозом, полученным методом экспресс-
тестирования. Кроме того, 12 из 16 модулей Xpert® не прошли
калибровку в течение 15 месяцев после начала использования.
Выводы Использование экспресс-тестов для диагностики
туберкулезаявляетсяперспективнымметодом,которыйсложно
реализовать с логистической точки зрения. Необходимы более
доступные и надежные платформы. Все пациенты с диагнозом
туберкулеза, в том числе те, у кого обнаружены резистентные
штаммы, должны начать и завершить лечение.
Resumen
Aplicación de la prueba de detección rápida de la tuberculosis en Mozambique
Situación En Mozambique, la tuberculosis pulmonar se diagnostica
principalmente mediante la baciloscopia del esputo. No obstante,
la sensibilidad de este método es insuficiente, especialmente en las
personasinfectadasconelvirusdelainmunodeficienciahumana(VIH).
Pocas veces se somete a los pacientes a pruebas para la tuberculosis
resistente a medicamentos.
Enfoque El programa nacional contra la tuberculosis y Health Alliance
International han introducido la prueba rápida de muestras de esputo
de frotis negativo. Se analizaron las muestras mediante un análisis
basado en la reacción en cadena de la polimerasa que detecta el ácido
desoxirribonucleicodelaMycobacteriumtuberculosisyunamutaciónque
indicaresistenciaalarifampicina;Xpert®MTB/RIF(Xpert®).Seinstalaron
cuatro máquinas en cuatro hospitales públicos junto con un sistema de
transportedeesputoparatransferirlasmuestrasdeloscentrosdesalud
seleccionados. Se capacitó a los técnicos de laboratorio para operar las
máquinas y a los médicos se les enseñó a interpretar los resultados.
Marco regional En 2012, Mozambique presentó aproximadamente
140 000 casos nuevos de tuberculosis, de los cuales solo se diagnosticó
y trató el 34 %. De los enfermos de tuberculosis, 58% está infectado por
elVIH.
Cambios importantes Entre 2012 y 2013, se diagnosticaron 1558
afectados nuevos por tuberculosis por medio del frotis de esputo en
los centros de intervención. Xpert® detectó la M. tuberculosis en 1081
muestrasadicionales,loquerepresentaunaumentodel69%.Sedetectó
resistenciaalarifampicinaen58delas1081muestras(5%).Sinembargo,
el tratamiento solo se inició en el 82 % de los pacientes diagnosticados
porbaciloscopiayenel67%delospacientesdiagnosticadosmediante
la prueba rápida. Hubo fallos de calibración en doce de los 16 módulos
de Xpert® a los 15 meses de la aplicación.
Lecciones aprendidas El uso de pruebas rápidas para diagnosticar
la tuberculosis resulta prometedor, pero es difícil desde el punto de
vista. Se requieren plataformas más asequibles y duraderas. Todos los
pacientesdiagnosticadoscontuberculosisdebeniniciarycompletarun
tratamiento, incluidos aquellos con cepas resistentes a medicamentos.
Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560130
Lessons from the field
Rapid testing for tuberculosis, Mozambique James Cowan et al.
References
1.	 Chaisson RE, Martinson NA. Tuberculosis in Africa–combating an HIV-driven
crisis. N Engl J Med. 2008 Mar 13;358(11):1089–92. doi: http://dx.doi.
org/10.1056/NEJMp0800809 PMID: 18337598
2.	 Ramsay A, Cuevas LE, Mundy CJ, Nathanson CM, Chirambo P, Dacombe R,
et al. New policies, new technologies: modelling the potential for improved
smear microscopy services in Malawi. PLoS ONE. 2009;4(11):e7760. doi:
http://dx.doi.org/10.1371/journal.pone.0007760 PMID: 19901989
3.	 Boehme CC, Nabeta P, Hillemann D, Nicol MP, Shenai S, Krapp F, et al.
Rapid molecular detection of tuberculosis and rifampicin resistance. N
Engl J Med. 2010 Sep 9;363(11):1005–15. doi: http://dx.doi.org/10.1056/
NEJMoa0907847 PMID: 20825313
4.	 Rachow A, Zumla A, Heinrich N, Rojas-Ponce G, Mtafya B, Reither K, et al.
Rapid and accurate detection of Mycobacterium tuberculosis in sputum
samples by Cepheid Xpert MTB/RIF assay–a clinical validation study.
PLoS ONE. 2011;6(6):e20458. doi: http://dx.doi.org/10.1371/journal.
pone.0020458 PMID: 21738575
5.	 O’Grady J, Bates M, Chilukutu L, Mzyece J, Cheelo B, Chilufya M, et al.
Evaluation of the Xpert MTB/RIF assay at a tertiary care referral hospital in a
setting where tuberculosis and HIV infection are highly endemic. Clin Infect
Dis. 2012 Nov;55(9):1171–8. doi: http://dx.doi.org/10.1093/cid/cis631 PMID:
22806590
6.	 Tuberculosis diagnostics Xpert MTB/RIF Test October 2013. Geneva:
World Health Organization; 2014. Available from: http://www.who.int/tb/
publications/Xpert_factsheet.pdf [cited 2014 Nov 21].
7.	 Negotiated prices for Xpert® MTB/RIF and FIND country list [Internet].
Geneva: FIND; 2014. Available from: http://www.finddiagnostics.org/about/
what_we_do/ successes/find-negotiated-prices/xpert_mtb_rif.html [cited
2014 Nov 21].
8.	 Global tuberculosis report 2013. Geneva: World Health Organization; 2013.
9.	 Global Health Observatory Data Repository, Mozambique country statistics
[Internet]. Geneva: World Health Organization; 2014. Available from: http://
apps.who.int/ghodata/?vid=14200&theme=country [cited 2014 Nov 21].
10.	 Relatório de actividades desenvolvidas durante o ano de 2013. Maputo:
Ministry of Health; 2014. [Portuguese].
11.	 Creswell J, Codlin AJ, Andre E, Micek MA, Bedru A, Carter EJ, et al. Results
from early programmatic implementation of Xpert MTB/RIF testing in nine
countries. BMC Infect Dis. 2014;14(1):2. doi: http://dx.doi.org/10.1186/1471-
2334-14-2 PMID: 24383553
12.	 Definitions and reporting framework for tuberculosis, 2013 revision.
Geneva: World Health Organization; 2013.
13.	 Cowan JF, Manhiça I, Michel C, Gloyd S, Creswell J, Macek C, et al. A
brief review of remote monitoring tools for GeneXpert MTB/RIF: Initial
implementation of GxAlert in Mozambique. Int J Tuberc Lung Dis. 2014
Nov;18(11 Suppl 1):S512–3.

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Implementing rapid testing for tuberculosis in Mozambique

  • 1. Bull World Health Organ 2015;93:125–130 |doi: http://dx.doi.org/10.2471/BLT.14.138560 Lessons from the field 125 Implementing rapid testing for tuberculosis in Mozambique James Cowan,a Cathy Michel,a Ivan Manhiça,b Claudio Monivo,a Desiderio Saize,a Jacob Creswell,c Stephen Gloyda & Mark Miceka Introduction People infected with human immunodeficiency virus (HIV) are susceptible to tuberculosis. This has led to an HIV-driven tuberculosis epidemic in sub-Saharan Africa over the past two decades.1 Diagnosing tuberculosis is often difficult given the low sensitivity of smear microscopy. Among people infected with HIV, smear microscopy is even less sensitive due to the lower bacterial load in co-infected individuals.2 Xpert® MTB/RIF (Xpert®; Cepheid, Sunnyvale, United States of America) is a rapid and fully-automated molecular test that uses real-time polymerase chain reaction on sputum samples to simultaneously detect Mycobacterium tuberculosis deoxyribonucleic acid and the genetic sequence indicative of rifampicin resistance.3,4 The test has 88% sensitivity for tuber- culosis and 94% sensitivity for rifampicin resistance. Given the high sensitivity, the test is more effective than sputum smear microscopy in diagnosing tuberculosis in HIV-infected people. Therefore the World Health Organization (WHO) has recom- mended the use of Xpert® for diagnosis of tuberculosis in coun- tries with high prevalence of HIV infection and multi-drug resistant tuberculosis (MDR-TB).5,6 The four-module Xpert® machine and desktop computer retails for 17 000 United States dollars (US$) in low-income countries and each cartridge (one per sample) costs an additional US$ 10.7 This paper describes the introduction of Xpert® in Mozambique. Local setting Mozambique has a high burden of tuberculosis. In 2012, WHO estimated an incidence of 552 per 100 000 people, which corresponds to approximately 140 000 new cases. However, only 34% of these estimated cases are diagnosed and notified to the national tuberculosis programme. Most, (94%), new tuberculosis patients are tested for HIV8 and 58% are found to be co-infected. Tuberculosis diagnosis is done in people reporting a persistent cough, using smear microscopy on sputum samples.8 MDR-TB testing is seldom done since culture of M. tuberculosis is not routinely available.8 New cases typically receive first-line therapy. The treatment success rate is 85% for new sputum smear-positive patients who start treat- ment at a public treatment centre.9 First-line therapy typically includes isoniazid, rifampicin, pyrazinamide and ethambutol. Second-line therapy typically includes kanamycin, levofloxa- cin, ethionamide, cycloserine, ethambutol and pyrazinamide. In 2012, an estimated 3.5% (4900 people) of the new estimated tuberculosis patients had MDR-TB; however, only 213 patients with MDR-TB started appropriate second-line treatment.8 Both in Mozambique and globally, the prevalence of MDR-TB tuberculosis is increasing. Therefore improved MDR-TB diagnostics and access to treatment are priorities for the Mozambican national tuberculosis programme and the global health community.8 Planned intervention To increase the number of people diagnosed and treated with tuberculosis and to improve MDR-TB detection and treatment, the Xpert® implementation project was approved by the Mozambican Ministry of Health, with support from Health Alliance International. We chose to use a two-step testing algorithm for individuals suspected of having pulmo- Problem In Mozambique, pulmonary tuberculosis is primarily diagnosed with sputum smear microscopy. However this method has low sensitivity,especiallyinpeopleinfectedwithhumanimmunodeficiencyvirus(HIV).Patientsareseldomtestedfordrug-resistanttuberculosis. Approach The national tuberculosis programme and Health Alliance International introduced rapid testing of smear-negative sputum samples. Samples were tested using a polymerase-chain-reaction-based assay that detects Mycobacterium tuberculosis deoxyribonucleic acid and a mutation indicating rifampicin resistance; Xpert® MTB/RIF (Xpert®). Four machines were deployed in four public hospitals along with a sputum transportation system to transfer samples from selected health centres. Laboratory technicians were trained to operate the machines and clinicians taught to interpret the results. Local setting In 2012, Mozambique had an estimated 140 000 new tuberculosis cases, only 34% of which were diagnosed and treated. Of tuberculosis patients, 58% are HIV-infected. Relevant changes From 2012–2013, 1558 people were newly diagnosed with tuberculosis using sputum smears at intervention sites. Xpert® detected M. tuberculosis in an additional 1081 sputum smear-negative individuals, an increase of 69%. Rifampicin resistance was detected in 58/1081 (5%) of the samples. However, treatment was started in only 82% of patients diagnosed by microscopy and 67% of patients diagnosed with the rapid test. Twelve of 16 Xpert® modules failed calibration within 15 months of implementation. Lessons learnt Using rapid tests to diagnose tuberculosis is promising but logistically challenging. More affordable and durable platforms areneeded.Allpatientsdiagnosedwithtuberculosisneedtostartandcompletetreatment,includingthosewhohavedrugresistantstrains. a Health Alliance International, 1107 NE 45th Street, Suite 350, Seattle, 98105, United States of America. b Mozambican National Tuberculosis Control Programme, Maputo, Mozambique. c Stop TB Partnership, World Health Organization, Geneva, Switzerland. Correspondence to James Cowan (email: jcowan22@uw.edu). (Submitted: 2 April 2014 – Revised version received: 8 November 2014 – Accepted: 11 November 2014 – Published online: 26 November 2014 ) Lessons from the field
  • 2. Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560126 Lessons from the field Rapid testing for tuberculosis, Mozambique James Cowan et al. nary tuberculosis. All sputum samples were analysed using smear microscopy and new patients with at least one posi- tive sputum smear out of two separate samples were treated with first-line tuberculosis therapy. Patients with two separate smear negative results were retested using Xpert® on one of the original samples. In the beginning of February 2012, four Xpert® machines were deployed at two district and two urban public hospi- tals in four districts in Sofala and Manica provinces. We developed a transporta- tion network to transfer smear negative sputum samples from three of the 10 surrounding health centres to the two urban hospitals. Eight remote health facilities routinely transferred samples to the two district hospitals via exist- ing sputum transport networks. This covered approximately 5% of all sputum samples tested in Mozambique.10 Initial training and technical sup- port for clinicians and laboratory staff in the four hospitals was led by Health Alliance International. Prior to Xpert® testing initiation, each site was given a day-long training session to train laboratory technicians to operate the machines and teach clinicians to in- terpret the results. Initial introductory meetings were also held with district and provincial ministry of health staff and supervisors. Health Alliance In- ternational trainers then provided at least weekly supervision visits to each site with focused training for techni- cians with elevated testing error rates, to troubleshoot problems, to review cartridge procurement and distribution and to undertake initial calibration. The trainers also monitored the testing care cascade to ensure that patients received their test results and were linked to ap- propriate treatment. Daily Xpert® testing and long-term management – such as technical support, cartridge procure- ment and routine maintenance – was assumed by the Ministry of Health after appropriate training. The national tuberculosis pro- gramme registers new tuberculosis pa- tients as either sputum smear negative or positive. The system has no capacity to record molecular test results. Therefore, laboratories using the rapid tests were instructed to report patients testing positive with Xpert® as sputum smear negative cases. However, this instruc- tion was not always followed and an estimated 5–10% of sputum smear nega- tive cases that tested positive on Xpert® were reported as sputum smear positive. The performance of this project was monitored from reports gener- ated from individual Xpert® machines. These reports were collected by hand each month, and information extracted included the number of tests run per quarter, a summary of the results, and lists of patients that tested positive, which were reconciled with the tuber- culosis treatment registries. This was combined with quarterly data from the national tuberculosis programme on the reported number of sputum smears analysed and the number of patients started on tuberculosis treatment. Xpert® was approved for general use by the Mozambican Ministry of Health and the national tuberculosis programme formally approved the implementation of this project. This implementation project was not a formal research study thus the University of Washington institutional review board declined to provide a full review of this proposal. Implementation and results From 1 January 2012 to 31 December 2012; 1558/12 509 (12%) people tested at the four hospitals had sputum smear positive results. Of the 10 951 people with sputum smear negative results, 8631 (79%) were tested using Xpert® and 1081 (13%) were positive for tuber- culosis. Thus, during this intervention Xpert® testing increased the diagnosis of bacteriologically-confirmed pulmo- nary tuberculosis by 1081/1558 (69%). Rifampicin resistance was detected in 58/1081 (5%) samples. Overall, 1019 (12%) of tests failed because of machine errors, and invalid or no results due to energy shortages. We reviewed the records of 445 newly-diagnosed patients from the four hospitals in the second quarter of 2012 and found that 26% [115/445] had not been started on treatment (18% [35/200] of those diagnosed by microscopy and 33% [80/245] diagnosed using Xpert®). For patients with rifampicin resistance, 53% [31/58] were not started on second- line treatment. Three patients with rifampicin resistance were mistakenly initially started on first-line treatment but were converted to second-line treatment. During 2012, 5076 people were placed on treatment in the four interven- tion districts, an increase of 632 patients (14.2%) over the baseline yearly aver- age for these districts which was 4444 patients (15 554 patients were treated in these districts during the 3.5 years before implementation). Challenges Despite encouraging outcomes, there were several programmatic and op- erational challenges in implementing and maintaining the Xpert® machines (Table 1). One computer failed within six months, despite being attached to a surge protector/current stabilizer. Twelve of the original 16 (75%) Xpert® modules broke or failed calibration within 15 months and had to be re- placed. In early 2013, Xpert® cartridges and calibration kits were back-ordered, resulting in several days without Xpert® cartridges despite ample lead-time in ordering.11 Updating antivirus software and operating systems and transferring data from the local computer to Cepheid in California, USA, was also difficult. Cepheid depends on Xpert® machines being connected to the internet to be able to diagnose problems remotely – this was not feasible in Mozambique and caused significant delays. Over time, shipments of cartridges and customer service improved as Cepheid employees and our team learned how to work with each other. However, importing con- sumables to Mozambique and clearing customs remained challenging, expen- sive and time-consuming. The lack of a notification system to report positive Xpert® results to the national tuberculosis programme and no ability to automatically upload re- sults electronically to a central secure database made it challenging to assess the impact of this intervention. It was difficult to remotely monitor Xpert® test- ing and notify key individuals in a timely fashion – such as provincial MDR-TB care coordinators when a patient tested positive for rifampicin resistance. WHO guidance on recording and reporting test results should allow national tuber- culosis programmes to better monitor performance.12 The current two-step testing algo- rithm likely caused delays in tuberculo- sis diagnosis relative to using Xpert® as a first-line test. Some patients returned after 24 hours for their smear results, but did not get their subsequent Xpert®
  • 3. Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560 127 Lessons from the field Rapid testing for tuberculosis, MozambiqueJames Cowan et al. result. The need for repeat visits to establish a diagnosis may have led to higher pretreatment loss to follow-up. In the beginning, sites did not routinely collect patient contact information so it was impossible to reach these primary defaulters. Initially there was no proto- col to routinely reconcile laboratory and treatment registries to ensure that all pa- tients diagnosed with tuberculosis were started on treatment. Efforts are ongo- ing to improve the entire tuberculosis care cascade and to increase treatment initiation rates. Lessons learnt Our small-scale implementation proj- ect allowed us to gain important prac- tical experience about the strengths and limitations of this new diagnostic technique (Box 1). Rapid tests have the potential to improve the diagnosis of tuberculosis and identify drug resis- tance. However, the tools are expensive and we experienced problems with the machines, data transfer, linkage to tuberculosis treatment initiation, reporting and follow-up. If the use of rapid diagnostic tests for tuberculosis is expanded to the national level, system improvements are needed to prevent these problems from occurring at a larger scale. The national tuberculosis pro- gramme is committed to effective care of all tuberculosis patients in Mozam- bique. Improving diagnosis is a part of this commitment and, therefore, rapid tests like Xpert® will be provided to more health centres. However, afford- able and durable tuberculosis diag- nostic platforms that can handle the stresses of laboratory environments in low-resource settings are still needed. Table 1. Responses to technical and logistical challenges encountered when implementing rapid tests for tuberculosis, Mozambique 2012–2013 Challenge Reason Response High testing error rates Laboratory technicians unfamiliar with Xpert® Targeted training of technicians at facilities with high error rates. Error rate decreased from 12% in first year to 6% in the second year Higher (20%) cartridge error rates when cartridges were stored in non-air conditioned rooms Installed air conditioners in cartridge storage areas Loss to follow-up Laboratory registries were not routinely reconciled with tuberculosis treatment registries Developed monthly meetings to reconcile laboratory and treatment registries Current two-step testing algorithm for tuberculosis delays patient results, decreasing the percentage of patients started on tuberculosis treatment Ensured that laboratories collect patient addresses and phone numbers Used existing community health workers to find and treat defaulters Start using Xpert® as a first-line test for high risk patients (those with HIV infection, diabetes, cancer, children) and those at risk for MDR-TB Loss to follow-up for patients with rifampicin resistance Some technicians did not initially understand that Xpert® tested for tuberculosis and rifampicin resistance Additional staff education Pilot a remote monitoring system to immediately notify key individuals by SMS when a patient tests positive for rifampicin resistance Lack of real-time monitoring and evaluation Xpert® originally designed to transmit data via Ethernet cables, not cell phone- based data connections that are widely available in low-income countries Ministry of Health and national tuberculosis programme reporting systems need to be adapted to incorporate test results Limited ability to access test results and aggregate these by district, province or national level Pilot a remote monitoring system for Xpert® that automatically transmits test results to a central database Determining an appropriate testing algorithm Balancing the high cost of Xpert® with increased sensitivity for detecting tuberculosis and rifampicin resistance Start using Xpert® as a first-line test for high risk patients (those with HIV infection, diabetes, cancer, children) and those at risk for MDR-TB Xpert® durability Poor understanding of routine maintenance requirements in dusty, non-temperature controlled remote laboratories Use Xpert® at health centres with adequate staff and maintenance support Develop maintenance protocols specific to remote laboratories in Mozambique Lusophone staff struggling with English software Software was initially only available in English A new version was released that supports several languages, including Portuguese HIV: human immunodeficiency virus; MDR-TB: multi-drug resistant tuberculosis; SMS: short message service. Box 1. Summary of main lessons learnt • Xpert® MTB/RIF (Xpert®) testing increased the number of confirmed bacteriologically positive tuberculosis cases. However, one third of patients diagnosed by Xpert® did not receivetuberculosistreatment,highlightingtheneedtostrengthentheoveralltuberculosis care cascade. • ImplementationandmaintenanceofXpert®machinesarecostlyandlogisticallychallenging, which creates a need for more affordable and durable molecular testing platforms. • Of the tuberculosis patients diagnosed with Xpert®, 5% were resistant to rifampicin, highlighting the need to develop a multi-drug resistance tuberculosis programme in Mozambique.
  • 4. Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560128 Lessons from the field Rapid testing for tuberculosis, Mozambique James Cowan et al. ‫ملخص‬ ‫موزامبيق‬ ‫يف‬ ‫للسل‬ ‫الرسيع‬ ‫االختبار‬ ‫تنفيذ‬ ‫رئييس‬ ‫بشكل‬ ،‫موزامبيق‬ ‫يف‬ ،‫الرئوي‬ ‫السل‬ ‫تشخيص‬ ‫يتم‬ ‫املشكلة‬ ‫هذا‬ ‫ولكن‬ .‫البلغم‬ ‫لطاخة‬ ‫باستخدام‬ ‫املجهري‬ ‫الفحص‬ ‫طريق‬ ‫عن‬ ‫األشخاص‬ ‫لدى‬ ‫سيام‬ ‫ال‬ ،‫منخفضة‬ ‫بحساسية‬ ‫يتمتع‬ ‫األسلوب‬ ‫فحص‬ ‫يتم‬ ‫ما‬ ً‫ا‬‫ونادر‬ .‫البرشي‬ ‫املناعي‬ ‫العوز‬ ‫بفريوس‬ ‫املصابني‬ .‫لألدوية‬ ‫املقاوم‬ ‫بالسل‬ ‫اإلصابة‬ ‫لتحديد‬ ‫املرىض‬ ‫الدويل‬ ‫والتحالف‬ ‫السل‬ ‫ملكافحة‬ ‫الوطني‬ ‫الربنامج‬ ‫قام‬ ‫األسلوب‬ .‫للطاخة‬ ‫اإلجيابية‬ ‫البلغم‬ ‫لعينات‬ ‫الرسيع‬ ‫االختبار‬ ‫بتنفيذ‬ ‫للصحة‬ ‫البوليمرياز‬ ‫تفاعل‬ ‫عىل‬ ‫يستند‬ ‫اختبار‬ ‫باستخدام‬ ‫العينات‬ ‫اختبار‬ ‫وتم‬ ‫الريبي‬ ‫واحلمض‬ ‫السلية‬ ‫املتفطرة‬ ‫البكرتيا‬ ‫يكشف‬ ‫الذي‬ ‫املتسلسل‬ ‫إىل‬ ‫تشري‬ ‫التي‬ ‫الريفامبيسني‬ ‫ومقاومة‬ ‫األكسجني‬ ‫منزوع‬ ‫النووي‬ Xpert® MTB/RIF”“ ‫السل‬ ‫داء‬ ‫واختبار‬ ‫طفرة؛‬ ‫حدوث‬ ‫عمومية‬ ‫مستشفيات‬ ‫أربعة‬ ‫يف‬ ‫أجهزة‬ ‫أربعة‬ ‫نرش‬ ‫وتم‬ .)®(Xpert .‫املختارة‬ ‫الصحية‬ ‫املراكز‬ ‫من‬ ‫العينات‬ ‫لنقل‬ ‫البلغم‬ ‫نقل‬ ‫نظام‬ ‫مع‬ ‫اخلرباء‬ ‫وتثقيف‬ ‫األجهزة‬ ‫تشغيل‬ ‫عىل‬ ‫املختربات‬ ‫فنيي‬ ‫تدريب‬ ‫وتم‬ .‫النتائج‬ ‫تفسري‬ ‫عىل‬ ‫الرسيريني‬ ‫يف‬ ‫اجلديدة‬ ‫السل‬ ‫حاالت‬ ‫بلغت‬ ،2012 ‫عام‬ ‫يف‬ ‫املحلية‬ ‫املواقع‬ ‫تشخيص‬ ‫يتم‬ ‫ومل‬ ،‫حالة‬ 140000 ‫التقديرات‬ ‫وفق‬ ‫موزامبيق‬ ‫مرىض‬ ‫من‬ ‫املائة‬ ‫يف‬ ‫ستني‬ ‫نسبة‬ ‫وكانت‬ .‫منها‬ % 34 ‫سوى‬ ‫وعالج‬ .‫البرشي‬ ‫املناعي‬ ‫العوز‬ ‫بفريوس‬ ‫مصابة‬ ‫السل‬ ‫تشخيص‬ ‫تم‬ 2013 ‫عام‬ ‫إىل‬ 2012 ‫عام‬ ‫من‬ ‫الصلة‬ ‫ذات‬ ‫ات‬ ّ‫ر‬‫التغي‬ ‫يف‬ ‫البلغم‬ ‫لطاخات‬ ‫باستخدام‬ ‫بالسل‬ ً‫ا‬‫حديث‬ ً‫ا‬‫شخص‬ 1558 ‫إصابة‬ ‫السلية‬ ‫املتفطرة‬ ‫البكرتيا‬ ®Xpert ‫اختبار‬ ‫وكشف‬ .‫التدخل‬ ‫مواقع‬ ‫مقاومة‬ ‫كشف‬ ‫وتم‬ .% 69 ‫نسبتها‬ ‫بزيادة‬ ،‫إضافية‬ ‫عينة‬ 1081 ‫يف‬ ‫تم‬ ،‫ذلك‬ ‫ومع‬ .‫العينة‬ ‫من‬ )% 5( 1081/58 ‫يف‬ ‫الريفامبيسني‬ ‫عن‬ ‫تشخيصهم‬ ‫تم‬ ‫الذين‬ ‫املرىض‬ ‫من‬ ‫فقط‬ % 82 ‫يف‬ ‫العالج‬ ‫بدء‬ ‫تشخيصهم‬ ‫تم‬ ‫الذين‬ ‫املرىض‬ ‫من‬ % 67‫و‬ ‫املجهري‬ ‫الفحص‬ ‫طريق‬ ‫أصل‬ ‫من‬ ‫وحدة‬ ‫عرشة‬ ‫اثني‬ ‫وعجزت‬ .‫الرسيع‬ ‫االختبار‬ ‫باستخدام‬ ً‫ا‬‫شهر‬ 15 ‫غضون‬ ‫يف‬ ‫املعايرة‬ ‫عن‬ ®Xpert ‫الختبارات‬ ‫وحدة‬ 16 .‫التنفيذ‬ ‫من‬ ‫تشخيص‬ ‫يف‬ ‫الرسيعة‬ ‫االختبارات‬ ‫استخدام‬ ‫املستفادة‬ ‫الدروس‬ .‫اللوجستية‬ ‫الناحية‬ ‫من‬ ‫حتديات‬ ‫عىل‬ ‫ينطوي‬ ‫ولكنه‬ ‫واعد‬ ‫أمر‬ ‫السل‬ ‫وتتسم‬ ‫معقولة‬ ‫تكلفة‬ ‫ذات‬ ‫أكثر‬ ‫منصات‬ ‫إىل‬ ‫حاجة‬ ‫ثمة‬ ‫وتوجد‬ ‫بالسل‬ ‫إصابتهم‬ ‫تشخيص‬ ‫يتم‬ ‫الذين‬ ‫املرىض‬ ‫مجيع‬ ‫وحيتاج‬ .‫بالقوة‬ ‫بسالالت‬ ‫املصابني‬ ‫املرىض‬ ‫ذلك‬ ‫يف‬ ‫بام‬ ،‫وإمتامه‬ ‫العالج‬ ‫بدء‬ ‫إىل‬ .‫لألدوية‬ ‫مقاومة‬ 摘要 莫桑比克实施结核病快速检测 问题 在莫桑比克,肺结核主要使用痰涂片镜检确诊。 然而,这种方法灵敏度较低,特别是在病人感染了艾 滋病病毒(HIV)的时候。患者很少接受耐药结核病 检测。 方法 国家结核病项目和国际健康联盟推出使用涂片 阴性痰标本的快速检测。样品使用以聚合酶链反应 为基础的化验进行检测,该化验为 Xpert®MTB/RIF (Xpert®),可发现分枝杆菌肺结核脱氧核糖核酸和指 示利福平抗性的突变。在四所公立医院部署了四台机 器和痰运输系统,以从选定的医疗中心转送样本。培 训实验室技术人员来操作这些机器并指导临床医生解 释结果。 当地状况 2012年,莫桑比克估计有14万名新结核病例, 其中只有 34% 接受诊断和治疗。58% 的结核病患者感 染艾滋病毒。 相关变化 从 2012 至 2013 年,在干预点通过痰涂片诊 断 1558 例新确诊结核病患者。Xpert® 在额外 1081 个 样本中发现结核分枝杆菌,增加达 69%。在这 1081 例 样本中有 58 例(5%)发现利福平抗性。然而,显微 镜诊断的患者中只有 82% 开始接受治疗,快速检测诊 断的患者中只有 67% 开始接受治疗。在实施的 16 个 月中,15 个 Xpert® 模块中有 12 个没有校准。 经验教训 使用快速检测来诊断肺结核是有希望的,但 在逻辑上具有挑战性。需要更多实惠且耐用的平台。 所有确诊患有肺结核的患者需要开始接受并完成治 疗,包括那些带有耐药菌株的患者。 Résumé Mise en œuvre d’un test de dépistage rapide de la tuberculose au Mozambique Problème Au Mozambique, la tuberculose pulmonaire est principalementdiagnostiquéeenexaminantdesfrottisd’expectoration aumicroscope.Cependant,cetteméthodeestpeusensible,enparticulier chezlespersonnesinfectéesparlevirusdel’immunodéficiencehumaine (VIH). Les patients sont rarement testés pour la tuberculose résistante aux médicaments. Approche Le programme national de lutte contre la tuberculose et Health Alliance International ont introduit le dépistage rapide sur les échantillonsdefrottisd’expectorationnégatifs.Leséchantillonsontété testésàl’aided’untestbasésurl’amplificationenchaîneparpolymérase, qui détecte l’acide désoxyribonucléique de la bactérie Mycobacterium tuberculosis et une mutation indiquant la résistance à la rifampicine: Remote monitoring and evaluation of rapid testing systems may improve with the use of platforms such as GxAlert, XpertSMS and the Cepheid cloud system.13 Finally, while innovation in diagnostic tests is important, this is only one part of the tuberculosis care cascade. When increasing the number of people diagnosed with tuberculosis, attention is needed to ensure they re- ceive the appropriate treatment, care and support. ■ Acknowledgement Health Alliance International is a centre within the Department of Global Health, University of Washington, Seattle, USA. Competing interests: None declared.
  • 5. Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560 129 Lessons from the field Rapid testing for tuberculosis, MozambiqueJames Cowan et al. Xpert®MTB/RIF(Xpert®).Quatremachinesontétédéployéesdansquatre hôpitauxpublicsavecunsystèmedetransportdesfrottisd’expectoration pourtransférerleséchantillonsdepuislescentresdesantésélectionnés. Les techniciens de laboratoire ont été formés à utiliser les machines et les cliniciens ont appris à interpréter les résultats. Environnement local En 2012, le nombre de nouveaux cas de tuberculose au Mozambique était estimé à 140 000, dont seuls 34% étaient diagnostiqués et traités. Des patients atteints de tuberculose, 58% étaient infectés par leVIH. Changements significatifs Depuis 2012–2013, 1558 personnes ont été nouvellement diagnostiquées comme tuberculeuses par examen desfrottisd’expectorationdanslessitesd’intervention.Xpert®adétecté M. tuberculosis dans 1081 échantillons supplémentaires, soit une augmentation de 69%. La résistance à la rifampicine a été détectée dans 58 des 1 081 échantillons (5%). Cependant, le traitement avait commencé chez seulement 82% des patients diagnostiqués par microscopieet67%despatientsdiagnostiquésparletestdedépistage rapide.Parmiles16 modulesXpert®,12 d’entreeuxn’avaientpasréussi l’étalonnage au cours des 15 mois de la mise en œuvre. Leçons tirées L’utilisation de tests de dépistage rapide pour diagnostiquer la tuberculose est prometteuse, mais reste difficile sur le plan logistique. Des plateformes plus abordables et durables sont nécessaires. Tous les patients diagnostiqués comme tuberculeux doivent commencer et terminer leur traitement, y compris ceux avec des souches résistantes aux médicaments. Резюме Применение метода экспресс-тестирования на туберкулез в Мозамбике Проблема Диагностика туберкулеза легких в Мозамбике в основном проводится методом микроскопии мазка мокроты. Однако этот метод имеет низкую чувствительность, особенно у людей, инфицированных вирусом иммунодефицита человека (ВИЧ). Пациенты редко проверяются на наличие лекарственно- устойчивого туберкулеза. Подход Национальная программа борьбы с туберкулезом и некоммерческая организация Health Alliance International внедрили метод экспресс-тестирования мазков мокроты с отрицательнымрезультатомпримикроскопии.Образцымокроты проверялись путем анализа на основе полимеразной цепной реакции,которыйопределяетналичиедезоксирибонуклеиновой кислоты Mycobacterium tuberculosis и мутации, указывающие на устойчивость к рифампицину. Данный экспресс-тест называется Xpert® MTB/RIF (Xpert®). В четырех государственных больницах были развернуты четыре установки и организована транспортная система для передачи образцов мокроты из избранных медицинских центров. Было проведено обучение лаборантов работе на данных установках и обучение врачей методу интерпретации результатов. Местные условия Согласно оценкам, в 2012 году в Мозамбике возникло примерно 140 000 новых случаев туберкулеза, лишь 34% из которых были диагностированы и вылечены. При этом 58% больных туберкулезом являются одновременно ВИЧ- инфицированными. Осуществленные перемены За период 2012-2013 гг. туберкулез был диагностирован у 1558 человек по результатам анализов мазков мокроты, проведенных в медицинских учреждениях. При анализе по методу Xpert® были обнаружены микобактерии в дополнительных 1081 образцах, что составляет увеличение на 69%.Устойчивостькрифампицинубылаобнаруженав58из1081 (5%) образцов.Однаколечениебылоначатотольковотношении 82%пациентовсдиагнозом,полученнымметодоммикроскопии, и 67% пациентов с диагнозом, полученным методом экспресс- тестирования. Кроме того, 12 из 16 модулей Xpert® не прошли калибровку в течение 15 месяцев после начала использования. Выводы Использование экспресс-тестов для диагностики туберкулезаявляетсяперспективнымметодом,которыйсложно реализовать с логистической точки зрения. Необходимы более доступные и надежные платформы. Все пациенты с диагнозом туберкулеза, в том числе те, у кого обнаружены резистентные штаммы, должны начать и завершить лечение. Resumen Aplicación de la prueba de detección rápida de la tuberculosis en Mozambique Situación En Mozambique, la tuberculosis pulmonar se diagnostica principalmente mediante la baciloscopia del esputo. No obstante, la sensibilidad de este método es insuficiente, especialmente en las personasinfectadasconelvirusdelainmunodeficienciahumana(VIH). Pocas veces se somete a los pacientes a pruebas para la tuberculosis resistente a medicamentos. Enfoque El programa nacional contra la tuberculosis y Health Alliance International han introducido la prueba rápida de muestras de esputo de frotis negativo. Se analizaron las muestras mediante un análisis basado en la reacción en cadena de la polimerasa que detecta el ácido desoxirribonucleicodelaMycobacteriumtuberculosisyunamutaciónque indicaresistenciaalarifampicina;Xpert®MTB/RIF(Xpert®).Seinstalaron cuatro máquinas en cuatro hospitales públicos junto con un sistema de transportedeesputoparatransferirlasmuestrasdeloscentrosdesalud seleccionados. Se capacitó a los técnicos de laboratorio para operar las máquinas y a los médicos se les enseñó a interpretar los resultados. Marco regional En 2012, Mozambique presentó aproximadamente 140 000 casos nuevos de tuberculosis, de los cuales solo se diagnosticó y trató el 34 %. De los enfermos de tuberculosis, 58% está infectado por elVIH. Cambios importantes Entre 2012 y 2013, se diagnosticaron 1558 afectados nuevos por tuberculosis por medio del frotis de esputo en los centros de intervención. Xpert® detectó la M. tuberculosis en 1081 muestrasadicionales,loquerepresentaunaumentodel69%.Sedetectó resistenciaalarifampicinaen58delas1081muestras(5%).Sinembargo, el tratamiento solo se inició en el 82 % de los pacientes diagnosticados porbaciloscopiayenel67%delospacientesdiagnosticadosmediante la prueba rápida. Hubo fallos de calibración en doce de los 16 módulos de Xpert® a los 15 meses de la aplicación. Lecciones aprendidas El uso de pruebas rápidas para diagnosticar la tuberculosis resulta prometedor, pero es difícil desde el punto de vista. Se requieren plataformas más asequibles y duraderas. Todos los pacientesdiagnosticadoscontuberculosisdebeniniciarycompletarun tratamiento, incluidos aquellos con cepas resistentes a medicamentos.
  • 6. Bull World Health Organ 2015;93:125–130|doi: http://dx.doi.org/10.2471/BLT.14.138560130 Lessons from the field Rapid testing for tuberculosis, Mozambique James Cowan et al. References 1. Chaisson RE, Martinson NA. Tuberculosis in Africa–combating an HIV-driven crisis. N Engl J Med. 2008 Mar 13;358(11):1089–92. doi: http://dx.doi. org/10.1056/NEJMp0800809 PMID: 18337598 2. Ramsay A, Cuevas LE, Mundy CJ, Nathanson CM, Chirambo P, Dacombe R, et al. New policies, new technologies: modelling the potential for improved smear microscopy services in Malawi. PLoS ONE. 2009;4(11):e7760. doi: http://dx.doi.org/10.1371/journal.pone.0007760 PMID: 19901989 3. Boehme CC, Nabeta P, Hillemann D, Nicol MP, Shenai S, Krapp F, et al. Rapid molecular detection of tuberculosis and rifampicin resistance. N Engl J Med. 2010 Sep 9;363(11):1005–15. doi: http://dx.doi.org/10.1056/ NEJMoa0907847 PMID: 20825313 4. Rachow A, Zumla A, Heinrich N, Rojas-Ponce G, Mtafya B, Reither K, et al. Rapid and accurate detection of Mycobacterium tuberculosis in sputum samples by Cepheid Xpert MTB/RIF assay–a clinical validation study. PLoS ONE. 2011;6(6):e20458. doi: http://dx.doi.org/10.1371/journal. pone.0020458 PMID: 21738575 5. O’Grady J, Bates M, Chilukutu L, Mzyece J, Cheelo B, Chilufya M, et al. Evaluation of the Xpert MTB/RIF assay at a tertiary care referral hospital in a setting where tuberculosis and HIV infection are highly endemic. Clin Infect Dis. 2012 Nov;55(9):1171–8. doi: http://dx.doi.org/10.1093/cid/cis631 PMID: 22806590 6. Tuberculosis diagnostics Xpert MTB/RIF Test October 2013. Geneva: World Health Organization; 2014. Available from: http://www.who.int/tb/ publications/Xpert_factsheet.pdf [cited 2014 Nov 21]. 7. Negotiated prices for Xpert® MTB/RIF and FIND country list [Internet]. Geneva: FIND; 2014. Available from: http://www.finddiagnostics.org/about/ what_we_do/ successes/find-negotiated-prices/xpert_mtb_rif.html [cited 2014 Nov 21]. 8. Global tuberculosis report 2013. Geneva: World Health Organization; 2013. 9. Global Health Observatory Data Repository, Mozambique country statistics [Internet]. Geneva: World Health Organization; 2014. Available from: http:// apps.who.int/ghodata/?vid=14200&theme=country [cited 2014 Nov 21]. 10. Relatório de actividades desenvolvidas durante o ano de 2013. Maputo: Ministry of Health; 2014. [Portuguese]. 11. Creswell J, Codlin AJ, Andre E, Micek MA, Bedru A, Carter EJ, et al. Results from early programmatic implementation of Xpert MTB/RIF testing in nine countries. BMC Infect Dis. 2014;14(1):2. doi: http://dx.doi.org/10.1186/1471- 2334-14-2 PMID: 24383553 12. Definitions and reporting framework for tuberculosis, 2013 revision. Geneva: World Health Organization; 2013. 13. Cowan JF, Manhiça I, Michel C, Gloyd S, Creswell J, Macek C, et al. A brief review of remote monitoring tools for GeneXpert MTB/RIF: Initial implementation of GxAlert in Mozambique. Int J Tuberc Lung Dis. 2014 Nov;18(11 Suppl 1):S512–3.