Journal of Clinical Tuberculosis and Other Mycobacterial Diseases

i An update to this article is included at the end
Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020) 100193
Contents lists available at
Journal of Clinical Tuberculosis and Other

Mycobacterial Diseases
journal homepage:
Understanding the gaps in DR-TB care cascade in Nigeria: A sequential

miXed-method study
Charity Oga-Omenka a, b, c,*, Jody Boffa d, e, Joseph Kuye f, Patrick Dakum g, h, Dick Menzies c, i,
Christina Zarowsky a, b, j
a
The School of Public Health of the University of Montreal (E´ SPUM), Montreal, Quebec, Canada
b
Centre de recherche en santé publique, Université de Montréal (CReSP), Canada
c
McGill University International TB Centre, Montreal, Quebec, Canada
d
Dahdaleh Institute for Global Health, York Univeristy, Toronto, Canada
e
Centre for Rural Health, School of Nursing and Public Health, College of Health Sciences, University of KwaZulu-Natal, Durban, South Africa
f
National Tuberculosis and Leprosy Control Program, Abuja, Nigeria
g
Institute of Human Virology, Nigeria
h
University of Maryland School of Medicine, Baltimore, MD, USA
i
Department of Epidemiology and Biostatistics, McGill University, Montreal, Canada
j
School of Public Health, University of the Western Cape, South Africa
A R T I C L E I N F O
A B S T R A C T
Keywords:
TB Care Cascade Background: Despite the availability of free drug-resistant tuberculosis (DR-TB) care in Nigeria since 2011, the
Nigeria country continues to tackle low case notification and treatment rates. In 2018, 11% of an estimated 21,000 cases
Access to healthcare were diagnosed and 9% placed on treatment. These low rates are nevertheless a marked improvement from
Drug-resistant tuberculosis 2015 when only 3.4% were diagnosed and 2.3% placed on treatment of an estimated 29,000 cases. This study de-
MiXed-methods scribes the Nigerian DR-TB care cascade from 2013 to 2017 and considers factors influencing gaps in care.
Diagnosis and treatment
Methods: Our study utilized a miXed-method design. For the quantitative component, we utilized the national
diagnosis and treatment databases, as well as the World Health Organization’s estimates for prevalence to
construct a 5-year care cascade: numbers of patients at each level of DR-TB care, including incident cases, in-
dividuals who accessed testing, were diagnosed, initiated treated and completed treatment in Nigeria between
2013 and 2017. Using retrospective data for patients diagnosed in 2015, we performed the Fisher ’s exact test to
determine the association between patient (age and gender) and provider/patient (region- north or south)
variables, permitting a closer look at the gaps in care revealed across the 5 years. Barriers to care were explored
using framework thematic analysis of 57 qualitative interviews and focus group discussions with patients,
including 5 cases not initiated on treatment from the 2015 cohort, treatment supporters, community members,
healthcare workers and program managers in 2017.
Results: A 5-year analysis of cascade of care data shows significant, but inadequate, increases in overall numbers
of cases accessing care. On average, between 2013 and 2017, 80% of estimated cases did not access testing; 75%
of those who tested were not diagnosed; 36% of those diagnosed were not initiated on treatment and 23% of
these did not finish treatment. In 2015, children and patients in Northern Nigeria had odds of 0.3 [95% CI 0.1–
0.7] and 0.4 [0.3–0.5] of completing treatment once diagnosed; while males were shown to have a 1.34
[95% CI 1.0–1.7] times greater chance of completing treatment after diagnosis. The main themes from quali-
tative data identified barriers to care along the care cascade at individual, family and community, as well as
health systems levels. At the individual level, a lack of awareness of the true cause of disease and the availability
of ‘free’ care was a recurring theme. Family interference was found to be a particular challenge for children and
women. At the health system level, low index of suspicion, lack of rapid diagnostic tools and human resource
shortages appeared to limit patients’ access.
Conclusions: Any gains in diagnostic technology and shorter regimens are lost with inadequate access to DR-TB
services. The biggest losses in the Nigerian cascade happen before treatment initiation. There is a need for urgent
* Corresponding author at: 7101, Parc avenue, 3rd floor, Montreal, Quebec H3N 1X9, Canada.
E-mail address: [email protected] (C. Oga-Omenka).
https://doi.org/10.1016/j.jctube.2020.100193
Available online 9 October 2020

2405-5794/© 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
C. Oga-Omenka et Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020)
action on identified gaps in the DR-TB cascade in order to improve care continuity at multiple stages, improve
health service delivery and facilitate TB control in Nigeria.
1. Introduction
providers as their first point of initial care-seeking for respiratory con-
Rifampicin- or multidrug-resistant tuberculosis (DR-TB) actively ditions and fever [13,14]. Patients, after onset of symptoms, visited
infected an estimated 484,000 people and took 214,000 lives in 2018, PMVs (79%), traditional healers (10%), and private hospitals (10%)
threatening to reverse years of advances in global TB prevention and [14]. Despite this, only 11% of total TB notifications come from the
control [1–3]. Drug resistance is an ongoing challenge, especially in private sector, or less than 3% of estimated incidence [13].
settings where healthcare systems are fragmented, suggesting gaps in Nigeria adopted the use of GeneXpert MTB/RIF (Xpert) technology
the care cascade [3,4]. in 2011 in several national reference laboratories, increasing access to
Nigeria accounts for 4% of the global DR-TB burden and 27% of the DR-TB diagnosis [15,16]. Prior to this, diagnosis for TB relied mostly on
incidence in Africa [3]. While the World Health Organization (WHO) smear microscopy, culture, molecular line probe assay and drug sus-
estimates that 4.3% of new and 15% of previously-treated people with ceptibility testing [7,17]. Initially, GeneXpert use was reserved for
TB in Nigeria have drug-resistant TB [3], others have suggested that the testing HIV patients, presumed DR-TB cases, children, and extra pul-
incident rate of DR-TB is much higher [5,6]. In a meta-analysis of 8,002 monary TB cases [18,19]. Treatment for DR-TB patients began with a
adult TB patients from across the country, Onyedum et al found 32% of hospital-based model in 2010 and evolved to include community-based
new (734/2892) and 53% of previously treated people (1467/5020) had DR-TB treatment initiation in 2013 [15,17]. By the end of 2015, the
DR-TB [5]. Gehre et al found 32% (9/28) and 66% (58/88) respectively country had scaled GeneXpert testing to 201 sites, from 7 sites in 2011,
in Lagos state [6]. expanded testing algorithms to include all presumed TB cases, imple-
Furthermore, Nigeria has particularly low notification and treatment mented DR-TB treatment in facilities within 16 States and community
rates of DR-TB. WHO estimates that only 11% of people with DR-TB DR-TB initiation in 27 States, with support from the Global Fund and
were diagnosed and 9% placed on treatment in 2018, compared to the other partners [17,18]. At the end of 2015, 12% of Gene Xpert sites and
39% diagnosis and 32% treatment rates globally [3]. The 2012 Nigerian 16% of DR-TB hospital bedspaces were in 3 privately owned facilities
National Survey found 75% of smear-positive cases presented with TB [18].
symptoms meeting the National criteria for screening (cough for two
2.1.2. Study data sources and contexts
weeks or more) who had not been previously diagnosed, reflecting some
The WHO TB estimates for Nigeria were derived from the 2012 Na-
missed opportunities for TB diagnosis [3,7]. According to the WHO,
tional TB prevalence and the 2010 DR-TB surveys, 2000–2008 notifi-
Nigeria contributes 12% of the global DR-TB diagnosis gap, defined as
cation data, and Standards and Benchmark Assessments for 2013 and
the gap between the number of new cases reported and the estimated
2017 [7,20–22]. Additional secondary quantitative data were derived
incident cases [3].
from national databases for diagnosis and treatment collected by the
In order to meet the End TB targets, Nigeria’s diagnosis rates and
National TB and Leprosy Control Program (NTBLCP) from public and
treatment coverage need to be 90% or more with a drug susceptibility
private facilities.
testing (DST) coverage of 100% [3]. The TB care cascade outlines a
The qualitative interviews were conducted in the South-West and
series of necessary steps and services each patient must go through to
North-Central geopolitical zones. Patient and provider interviews were
achieve a positive health outcome. This includes accessing testing,
conducted in 2017 from two of the largest DR-TB treatment centers in
receiving a diagnosis, initiating treatment, completing treatment and
Nigeria, with 48 and 34 beds, respectively: Sacred Heart Hospital (SHH)
surviving at one year of follow-up [8].
in Ogun State and the Jos University Teaching Hospital (JUTH) in
Identifying gaps in the DR-TB care cascade in a given setting enables
Plateau State. Two large treatment facilities were purposively selected
targeted interventions at the stages of the care cascade where losses and
to differ based on location and sector (one privately owned facility in the
drop-outs occur most frequently. Currently, information on factors
South – SHH; and a public facility in the North – JUTH) to maximise
contributing to gaps in DR-TB care in Nigeria is limited. Our study aimed
external validity.
to estimate the gaps along the DR-TB care cascade and to identify bar-
riers to care from the perspectives of patients, their relatives and DR-TB
care providers in Nigeria. 2.2. Study design and methods
2. Methodology Our sequential miXed-methods study (Fig. 1) utilised the following

methods: a review of Nigeria’s DR-TB cascade over 2013–2017 using
2.1. Study setting data from WHO Global TB Reports [20–24], a cohort analysis of patients
diagnosed in 2015, and a qualitative study based on semi-structured
2.1.1. National and TB program context individual interviews with a purposive sample of respondents. We
Nigeria, with an estimated 193 million people in 2016 [9], has 36 used the MiXed Methods Appraisal Tool (MMAT) [25] to
States and one Federal Capital Territory, across 6 geopolitical zones: conceptualize, develop and interpret findings from this study [26].
North-Central, North-East, North-West, South-East, South-South and The purpose of this sequential transformative miXed methods study
South-West [10]. In 2016, there were an estimated 34,140 health fa- [27] was to understand the health system and patient barriers and fa-
cilities in Nigeria- with 88% of them primary, 11% secondary and 0.13% cilitators to the DR-TB care cascade. The quantitative phase explored
tertiary [11,12]. Of these, 67% were public-funded and 33% private health system and patient factors associated with gaps in the DR-TB care
sector health facilities, excluding patent medicine vendors (PMVs) continuum. The qualitative phase enhanced the understanding of the
and private pharmacies [11]. In terms of geopolitical distribution of health system and patient-related factors for these gaps.
health facilities, the North-East had 18.6, North-West 14.4, North-
Central had 25.8, South-West 20.4, South-East 23.4 and South-South 2.3. Quantitative data collection and analysis
14.0 health
facilities/100,000 population [11]. The WHO TB Nigeria estimates used national TB prevalence (2012)
Although only 33% of treatment facilities were privately owned, and DR-TB (2010) surveys, Standard and Benchmark Assessment (2013,
studies found that 66–92% of the time, new TB patients visited private 2017), and TB notifications (2000–2018) [28]. We elected to analyse the
2
2015 cohort of diagnosed patients because this was the most recent year
sources of data are described in the Appendix.
with available, complete, cleaned and deduplicated treatment outcome
data from DR-TB in the national treatment register, allowing for further Our second approach is cohort-based, and is a denominator-
insights on gaps in care revealed across the 5 years. The primary results denominator linked method [8,30]. Recurrence-free survival was also
not included because of a lack of data. The additional retrospective data
of this analysis have been published elsewhere [29].
was collected from 2 different web-based databases for all patients
We used two approaches to describe the DR-TB care cascade ac-
diagnosed with DR-TB in 2015. The diagnosis (G XAlert) receives results
cording to categories outlined by Subbaraman [8]. As a first step, we
from Xpert machines on diagnosed patients. The e-TB Manager database
extracted the following data for Nigeria from annual WHO TB reports
has records for all patients placed on TB treatment. Treatment initiation
from 2013 to 2017 [20–24] utilising a denominator-numerator unlinked
records were tracked from January 2015 to August 2017 (20–32 months
methodology [8,30]: 1) Estimated DR-TB incident cases (defined by the
after diagnosis). Preparatory processes, including the handling of
WHO as the TB cases arising in a given time period, usually one year), 2)
missing data, have been discussed in a prior publication [29].
Number of individuals with DR-TB who accessed TB tests, 3) Number of
We utilised VassarStats, a computational statistics website, (www.
individuals with DR-TB who were successfully diagnosed as having drug-
vassarstats.net) to perform descriptive statistics and tests for associa-
resistant TB, 4) Number of individuals registered on DR-TB treatment
tion. We used Pearson’s chi-squared test to determine associations and
and 5) Number of patients who completed TB treatment. Recurrence-free
Fisher’s exact test to compare differences between categorical variables.
survival, the final step of the TB care cascade, was not included as there
was insufficient data to measure this. Unlike other years, DR-TB incident
cases for Nigeria were not explicitly stated in the WHO annual reports for 2.4. Qualitative data collection and analysis
2013 and 2014 [23,24]. Rather, we calculated DR-TB incidence based on
the 2.9% of new TB events estimated by the WHO for these years. Our qualitative study involved interviews of patients, relatives, and
National program data is disaggregated for age, sex and geopolitical providers in Ogun and Plateau states, as well as program managers in
zone. We used notification data to describe the same for incidence and Benue and Abuja, the Federal Capital Territory (FCT). A total of 57 in-
testing access [18]. The outcome indicators, including terviews were conducted in these States, including 10 focus group dis-
cussions (FGDs), 12 key informant interviews (KIIs) - including 5 phone
Fig. 1. MiXed-methods sampling strategy.
3
interviews - and 35 in-depth interviews (IDIs). The five [5] phone in-
study. An additional ethical approval was obtained from the Research
terviews were conducted using contact information for patients who
Ethics Committee (CER) of sciences and health of the University of
were diagnosed but whose treatment start dates were not found in the
Montreal (CERSES-19-098-D). All interview participants gave written or
treatment register to contrast with patients who were already on treat-
verbal informed consent.
ment. There were a total of 127 unique interviewees (Fig. 1).
We asked providers to describe the program structure, challenges
and strengths, as well as their perception of access barriers and facili- 3. Results
tators. Patients and their treatment supporters were asked to describe
barriers and facilitators to accessing DR-TB care that they, their relative 3.1. Quantitative results
or someone they knew had experienced. Community interviews
explored common beliefs and practices around TB among the general 3.1.1. Changes in DR-TB care cascade in Nigeria, 2013–2017
population. We grouped themes into the different stages of DR-TB care Our data shows an gradual increase in numbers retained across all
based on participants description of barriers and facilitators they faced stages of the cascade between 2013 and 2017. Graphs showing each
as they navigated the care process, although they were not specifically stage of the DR-TB care cascade from 2013 to 2017 are described in
asked to match these factors to all the stages. more detail below.
Government and program managers at the central level were asked Estimated incidence varied between 2013 and 2017 due to differ-
about national policies and resources available for DR-TB control and ences in measurements (AppendiX 1). According to the WHO, Nigeria DR-
how these resources were distributed nationally and within each State. TB incidence estimates fell from 29,000 in 2015 to 20,000 in 2016 (a
They were also asked about the strengths and challenges within the reduction of 32%) when data on the prevalence of HIV among prevalent
program and how these might have affected different groups of patients. TB cases derived from the 2012 national prevalence surveys from
All interviews were conducted between September and November Nigeria was used to re-estimate TB incidence ([21], p.24). We have
2017 by CO, using interview guides developed by the research team and elected to use a 5-year average of estimated incidence.
piloted at the beginning of the data collection. Initial entry meetings The increases in cases diagnosed and treated over the 5 years was
were held with national and state coordinators, as well as clinic man- statistically significant (p < 0.0001) (Fig. 2). In step 5, treatment success
agers at both treatment meetings to discuss overall objectives of the rate stayed relatively the same from 76.9% in 2013 to 76.7% in 2016.
research and sampling strategies. Participants were selected based on Data were unavailable on the number of patients diagnosed in 2017 who
their role in the DR-TB program and availability during the interview completed treatment.
timeframe. Informed consents were written or verbally acknowledged Percentage retained, which is the ratio between patients who
before each interview. All interviews with patients were conducted completed treatment and the estimated incidence for the year, increased
outdoors in the treatment centers with patients who had been on from 1.5% to 4.8% between 2013 and 2016, representing a 3-fold
increase.
treatment for more than two weeks. Interviews were conducted in En-
glish and respondents were encouraged to respond in or ask for trans- The percentage losses between each stage of care are shown in Fig. 3.
On average, between 2013 and 2016, 80% of estimated DR-TB
lation into Nigerian pidgin, Yoruba or Hausa as needed. Interviews were
patients did not gain access to testing for TB or drug susceptibility.
audio-recorded and transcribed. There were instances of responses
Three- quarters of those who were tested were never diagnosed. Of
translated from the Yoruba language, the predominant language in the
those diagnosed, 35% were not initiated on treated, and 23% of those
South West of Nigeria and pidgin English by translators fluent in those
languages. Transcripts were sent back to 17 participants who had earlier treated did not complete treatment. The biggest losses over these years
agreed to be contacted for accuracy checking. Si X participants respon- were in testing and diagnosis access, as more than 60% of those
ded, with 2 requesting minor revisions, and transcripts were revised diagnosed were treated, and went on to complete their treatment.
accordingly prior to analysis.
We used a framework approach involving both inductive and 3.1.2. Characteristics of patients within the DR-TB care cascade in 2015
deductive thematic analysis [31]. Codes were inductively derived and Data sources for the cascade steps and gaps for patients diagnosed in
assigned to new themes or deductively derived from themes identified 2015 are shown in Table 1.
from an initial systematic review of barriers and facilitators to DR-TB The DR-TB diagnosis and treatment data for 2015, disaggregated by
care [32]. Interviews were coded by the first author (CO) with the age, sex and geopolitical location, gives a closer look into the gaps in
help of 2 assistants. All themes and codes were double-checked by CO. care (Table 2). Among the 29,000 people estimated to have to TB of any
Other members of the research team checked the thematic analysis for form in 2015, 4700 were estimated as DR-TB cases among notified
overall alignment with study objectives. Transcripts were coded with aid pulmonary TB cases. The WHO estimates these as the DR-TB patients
of Quirkos software, version 1.6.1. expected to be found among all notified pulmonary TB patients for a
The research team comprised two senior scientists (CZ and DM) with given year, if all notified pulmonary TB patients were tested for RIF-
extensive experience in social, implementation science and TB research; resistance using WHO-recommended diagnostic tests [36]. This is
a PhD researcher (CO) and post-doctoral fellow (JB) with over 15 years different from the absolute number of patients tested for DR-TB (with or
of combined implementation and mi Xed-methods research experience in without a positive result) in the year. Subbaraman et al, 2019 [8]
HIV/AIDS and TB in sub-Saharan Africa; a DR-TB National program (Table 1) recommends using this estimate of DR-TB among notified
manager (JK), implementing partner and seasoned researcher in Nigeria pulmonary TB cases as a proXy for the total number of DR-TB patients
(PD); and a research assistant who was a recent science graduate fluent who likely accessed testing during the same period. Of these, 996 were
in Yoruba and the pidgin English widely spoken in Nigeria. The research diagnosed with DR-TB, 660 were treated and 511 completed treatment.
assistant was trained for 2 weeks on qualitative interview skills before The association between age, sex and geopolitical zone and pro-
fieldwork. None of the researchers were directly involved in patient gression through the cascade of care was shown to be statistically sig-
management for DR-TB. nificant. Using the Fisher’s exact probability test, children had lower
odds than adults (0.3, 95% CI 0.1–0.7), males had 1.34 (95% CI 1.0–1.7)
2.5. Ethics greater odds than females, and patients in the north had lower odds than
those in the south (0.4, 95% CI 0.3–0.5) to move from diagnosis to
The National Health Research Ethics Committee of Nigeria (NHREC/ treatment completion. A further analysis of this cohort are presented in a
previous publication [29].
01/01/2007) and the Research Ethics Committee (CER) of the Univer-
sity of Montreal Hospital (17.060) granted ethical approval for this
4
Fig. 2. Trends in DR-TB Care Cascade in Nigeria 2013–2017.
Fig. 3. Average Retention and Losses in DR-TB Care Cascade in Nigeria.
5
Table 1
Cascade step Estimation/data source (reference) DR-TB n (95% CI) Gap Interview data source
1. Estimated • WHO estimation based on country 29,000 1: Number of individuals with TB • Community members and families of
Incidence prevalence surveys [20]• National drug [15,000–43,000] who did not reach health individuals who died of probable DR-TB•
resistance survey (2010)• National TB facilities and access a TB Pathways of individuals on DR-TB treatment•
prevalence survey (2012) [7]• NTP program diagnostic test Providers of DR-TB care at the health center
data (2015) [18,33] and community levels
2. Accessed testing • Percentage notified for any TB who were 50,274 [–] 2: Number of individuals with TB • Community members and families of
for any TB tested for rifampicin resistance [20]• National who accessed a TB diagnostic individuals who died of probable DR-TB•
(reached TB reference laboratory data• NTP case test but did not get successfully Pathways of individuals on DR-TB treatment•
centre) notification data [18] diagnosed Providers of DR-TB care at the health center
• WHO TB estimate of DR-TB among notified 4700[3700–5700] and community levels
pulmonary TB cases [20]• NTP case
notification data [18]
3. Diagnosed • National Gene Xpert database [34]• NTP 996 [–] 3: Number of individuals • Gene Xpert (diagnosis) database• Individuals
case notification data [18] diagnosed with TB who did not on DR-TB treatment• Community members•
get initiated in treatment Providers of DR-TB care at the health center
and community levels
4. Initiated on • National e-TB (treatment) database 660 [–] 4: Number of individuals who did • Community members of individuals who did
treatment [35]• WHO [20] not complete TB treatment (due not complete DR-TB treatment• Providers of
to treatment failure, loss to DR-TB care at the health center and
follow-up, or death) community levels
5. Treatment 511 [–] 5: 5: Number of individuals who No data
• National e-TB (treatment) database
completed experienced post-treatment TB
[35]• WHO [20]
recurrence or death
Table 2
Characteristics of patients within each stage of the care cascade in 2015.
2
Characteristic *Estimated *Estimated Diagnosed Treated Completed Pearson X p- Diagnosed Vs Completed Fisher’s
exact test
Incidence Tested value
TOTAL n (%) n (%) n (%) n (%) n (%) OR [95% CI]
29,000 4700 996 660 511
Age Children 3316 (11.4) 248 (5.3%) 26 (2.6) 8 (1.2) 8(1.4) 0.0685 0.2989 [0.1287–0.6941]
(0–14)
Adults (>14) 25,686(88.6) 4453 (94.7) 970 652 580 (98.6)
(97.4) (98.8)
Sex Male 17,568 (60.6) 2882 (61.3) 647 (65.0) 444 398 (67.7) 0.4527 1.338 [1.028–1.741]
(67.3)
Female 11,432 (39.4) 1819 (38.7) 349 (35.0) 216 190 (32.3)
(32.7)
Geopolitical North 50,225 2606 460 239 206 0.0004 0.4032 [0.3118–0.5215]
region
South 40,359 2094 536 366 358
* Not included in the Pearson X2 test of association or the Fisher’s exact test as these numbers are estimates
3.2. Qualitative results “For me, when I started coughing, I was thinking that maybe it’s [a]
normal cough, two and three days, you use [cough syrup] and it will
3.2.1. Factors influencing gaps in care go…”.
Our qualitative analysis focused on the first four cascade of care steps
Others were unclear about where to get tested:
– testing access, diagnosis, treatment initiation and completion. From
the perspective of patients and treatment supporters, several factors “…this TB is killing people a lot. For many people that I know, realising
influenced access to care at each stage of the cascade. The interviews later that it was this sickness that killed [them], and they did not know of
with providers were mostly in agreement with the factors identified by this centre or to go to another centre” (Patients FGD).
patients and their relatives.
Our results presented below and in Fig. 4, group themes For many, initial care seeking involved alternatives to the public
influencing each stage of the care cascade into individual/patient sector. For example, many patients or their loved ones described first
factors, interpersonal influences operating at the family or seeking care through “prayer houses,” traditional healers, or through the
community level, and finally at the health system level. We present private sector:
several examples, especially for testing and diagnostic gaps, which
“[When this illness started], I went to private hospitals, and they did not
were identified as the major barriers in the quantitative results.
see anything wrong with me, I went to church and they said it was
spiritual attack. Then I went to a [health] centre and they were not
3.2.2. Gap 1: accessing to TB diagnostics
straight for- ward, they did not answer me. I started using different types
Many respondents described individual delays in accessing testing. of herbal mixture for like one month but I had gone round earlier before I
Predominantly, this related to a number of uncertainties about TB and to got here.” (Patients FGD)
symptom minimization, being unaware of available care and the use of
alternative care as a first option. For example, one FGD participant There were also instances of patients resisting further testing. One
indicated: healthcare worker described patient fears related to long hospital stays if
6
Fig. 4. Summary factors influencing DR-TB care cascade.
they were found to be positive: coughing for a week and I heard on radio that it is free in the hospital. It
will create awareness” (Patient FGD).
“We actually want[ed] him to come for [a drug resistance] test but some
other people [had] …cornered him [to say] by the time you go, they are Providers also reinforced the need for more awareness, similar to
going to put you in the treatment center and you may not come out till so, what exists in the HIV program.
so period, so the patient refused [to come back]”(HCW KII).
“One thing I can say is that, it is just the awareness, for [patients] to
When asked what could have helped them or their loved one get know that this TB has to be diagnosed and where to get the treatment… I
earlier access to testing, respondents indicated clearer information think that the major thing … that [TB] is existing, and [services] are
about TB and where to access reliable testing services at no cost to pa- free….…” (HCW KII).
tients. One family member described his perspective of care in private “…The awareness is not much, they should …make people aware of TB,
hospitals, where he felt his loved one had unnecessarily perished: like … they did for HIV. …the awareness is not as much as that of HIV.
And TB is killing more than HIV” (HCW KII).
‘The problems I have noticed are amongst the private hospitals. They
don’t diagnose [when] people have TB. They give wrong medications to Several family and community influences were reported to prevent
people with DR-TB, which worsens their cases. They will be treating access to testing. Respondents cited instances in which patients’ parents
malaria, typhoid [fever]… making some mistakes costing people their or spouses acted as a barrier to appropriate care, sometimes because of
lives. But, assuming the knowledge of TB is everywhere… it will be easy their own beliefs in alternate care, a lack of awareness about the TB
for [private hospitals] to diagnose and treat it” (Patient relative KII). symptoms or available services. These are discussed further in cross-
cutting themes below.
All participant groups repeatedly highlighted the need for increased
A number of health system barriers were identified including inade-
community awareness around TB and availability of free services.
quate coverage of services, inadequate human resource, lengthy care
“Before coming here I was not aware … that there is TB care here … procedures, and misdiagnosis due to low index of suspicion in both
[and] that everything is free. I didn’t believe that …my mummy asked if I public and private hospitals. The attitude of public healthcare workers
would come I said no, I was not coming but [eventually I came was also a cited as a barrier.
and].. [my health] has improved … The patients coming here are happy “The first day I went for [a] test….…they chased me out that I should go
… that is why we are suggesting radio advertisement or TV …” (Patient and stay by the window…I felt embarrassed ...why should I be disgraced
FGD). to stay outside ...they ordered me to buy [a] handkerchief to cover my
“My advice is that there should be awareness through the radio or tele- mouth … they chased me away” (Patients FGD).
vision that whoever that coughs should visit hospital that it is free because
when charges are involved many will run. Many listen to radio in car or
homes or television. [Someone can say], my friend you have been
7
3.2.3. Gap 2: from testing to diagnosis

Participants mentioned several patient-level reasons for difficulty There were particular instances of adult females living with their
getting diagnosed after testing. A predominant theme was preference for parents, who were prevented from accessing treatment. In one instance,
private sector care or long wait times for test results in the public sector, the duration of treatment was a barrier, and the parent thought going to
which led to the seeking of alternate care elsewhere. A second important a prayer house would bring faster results. In the other instance, the fa-
theme was not being able to pay transportation costs to return for ther believed his daughter was already healed by prayer and not in need
appointments. of any medication.
Family responsibilities and fear of separation, school and work
“I got there for sputum culture, at government hospital they said [for] this conflicts were also mentioned as barriers to starting treatment.
[test], you will have to come back for it. They will have to be giving us [a] At the health system level, limited hospital bed spaces to admit pa-
date to come back for the sputum, they will say come back another day, if tients in the initial phase of treatment contributed to delays in treat-
you get there again they will say you came late, and this thing is ment. HCWs also mentioned staff workload and low motivation, due to
disturbing me up to the extent that I could not walk, people will have to unpaid salaries, resulting in slow case management.
hold me, until they said go somewhere else” (Patients’ FGD).
“From the provider’s side is a lack of motivation. Imagine you are going
At the interpersonal level, there were instances of families removing to attend to a patient every day for … 20 months, that means you
patients from the care cascade to seek alternatives in traditional healing abandon almost all you have to do for that patient. And in a situation
and prayers, or the patients themselves preferring alternative care to the where salaries are not forthcoming and the support from the [funding]
DR-TB care offered publicly. These are discussed in cross-cutting themes partners are [much]. The program pays the DOTS providers [5USD]
below. While these family influences were sometimes negative, there communication allowance monthly but there is a very good package for
were also responses indicating that parents had to be persistent to get the patients [105 USD]. … Most of the providers in the face of no salaries
their children diagnosed. will … envy what the patients are getting… So, from the provider side
this is one of the major challenges” (HCW KII).
“They did [a] series of tests for her [daughter] and it was saying
negative, negative until that thing ate all her lungs and killed her. So,
when her [other daughter] started coughing, they were taking her to 3.2.5. Gap 4: from treatment initiation to treatment completion
several hospitals, until they got to general hospital …. [For] months, At the individual level, several respondents mentioned that adverse
they asked [the mother] to come back, … she was always going and drug reactions were a major issue with adhering to the treatment
coming, asking [about] the result [and] they always said nothing. [Much] regimen. These led to some instances of patients losing hope or
later, [they] called the mother [with the result]” (Patients FGD). becoming anxious and refusing further treatment or dying while on
treatment.
At the health system level, the predominant themes were prolonged
laboratory delays and errors, as well as negative healthcare worker “[An elderly man], … when he sees the tray for drugs, … he will start
attitudes. vomiting, ha! even when they have not given him, as soon as he sees it, he
starts vomiting. … even nurse or doctor, when he sees them he will just
“Sometimes [the problem] is waiting… you brought the sample and
start vomiting, and finally he said he wants to go, … if he even sees the
… most of time is the DOTS people will not give … accurate …
color of the doctors or nurses uniform he will be so afraid…he said it is
information. They [will] say …drop your sample in the lab .. and go and
better for him to go [home] and die… maybe he is dead but we don’t
… come back tomorrow or come back on Friday, [and] today is [only]
know… they gave him [the] paper to sign out of treatment…and he signed
Monday…[they will say] come back next week (HCW KII).
out and left” (Patients FGD).
“Some [government] hospitals …were always postponing appointments,
treating people like animals…they shout on us not to stand somewhere, An initial 8 months hospitalization was the standard practice before
touch anything, or …go out, come back tomorrow, up to the extent that I 2013 and is still used for certain high risk patients e.g. pediatric cases
had given up … but … a month after I got the test after disturbing them, and those who are pregnant or have co-morbidities. Transitioning be-
but some people do not have the perseverance to do what I did….…please tween the initial hospital phase and continuation in outpatient care was
help us to explain to [HCWs] to treat [patients] well” (Patients FGD). also another point at which patients dropped off treatment, sometimes
due to miscommunication or poor understanding of the process.
3.2.4. Gap 3: from diagnosis to treatment “…a lack of information caused my stopping the treatment, due to…
Barriers to treatment initiation occurred at individual, family and lapses on their sides… because … after they discharged me I was [told]
health system levels, many of which were also cross-cutting, such as to go [to] the community- who are the community I don’t know,…
preference for private sector care. At the individual level, some partic- [that] is their medical term…[I] am not a medical person. How do I get
ipants recalled knowing patients who died before they could initiate to know all those things? …that was how I actually stopped… taking my
treatment due to delayed diagnosis. A few instances were cited of pa- medication” (Patients FGD).
tients refusing treatment or giving false addresses because of fear of long
treatment duration or belief in alternative care, particularly traditional Weak linkages and referral systems led to patients dropping off
or spiritual healing. treatment when moving between facility and home. One instance
involved a prisoner released from jail who was subsequently lost to
“Sometimes … there are some people … they [say they] know what their follow-up.
problem is. [They] came to [the hospital but] gave [a] fake address and
phone number … I think this quarter alone … I have lost 3 [patients] like 3.2.6. Cross-cutting barriers across the care cascade
that. The last conversation we had was that they know their problem was Several cross-cutting barriers were identified. At the individual level,
[a spiritual attack] from their village and [they] are going to [the these included attributing symptoms to other causes or perceptions
church]. about healthcare which led to a preference for alternative care at all
… Sometimes [for this] group of people you cannot account for them, levels of the cascade.
because …when you call …the number will not connect” (HCW KII).
8
The major cross-cutting themes on interpersonal influences were

“…they are taking [good] care of us. We [get our medications] and
related to the influence of parents, spiritual leaders and to a lesser de-
collect injections at the right time; if anything happens to us or we feel
gree, husbands. Although predominantly negative, these experiences
anything, we go to meet them. They [joke] with us, allowing us to realise
were sometimes positive.
that we are still humans and that there is still hope for us here…”
“My pastor, he told me to come to the [treatment center], that this cough I (Patients FGD). “They attend to us as if we are their [relatives]. There
am coughing that he has seen someone that was coughing the same is no stigmatisa- tion… I don’t know of other centres but they don’t
and had been collecting drugs for six month and it stopped.It was my separate themselves [from us here]. If at times we [don’t] use our
pastor that knew about it and ask me to come.” (Patients FGD). mask, they talk to us …, attend to us. They don’t … shout at us [or]
“We have had a case of a pastor who refused … a member of his church make us feel different” (Patients FGD).
from taking drugs for DR-TB when the patient actually has DR-TB. He
refused vehemently that it was not a disease to be cured like that, that it The provision of free DR-TB care and patient financial support was
was a special [problem]. But … eventually [the pastor] himself came mentioned repeatedly by patients and their relatives as the main facil-
down with DR-TB and died” (HCW KII). itator to care.
Parental influence was a particular problem across the care cascade, “…when I remember [what I went] through [with] my daughter, how they
affecting even adult patients, especially if they were female. This was [referred] us from [one hospital] to [another]. [An] ordinary razor
often due to the parents own perception of better results with alternative blade, before they will give you … you go and pay in to the [hospital]
care. account … but, I thank God for [the program]. They make me to be the
happiest woman on this earth because [to] lose a child of … 15 years
“I had an experience….… a patient ... was ... asked ..to go and do... a [would] not [have been] easy but today they put laughter into my own
[further testing] ….the mother insisted that it is ...a spiritual attack...and family… Thank you.” (Treatment supporters FGD).
all effort to ensure that.. the patient takes treatment, failed” (HCW KII). “The day they gave me the result and said it was TB, I was like ah, and I
started thinking that where do I want to get money, I told my husband and
In one instance, a phone interview was cut short when the partici-
he was worried. The doctor then said that whatever we are using here will
pant, who had not yet initiated treatment, was interrupted by her father,
be free of charge…” (Patient FGD).
who cut the line after demanding that the interviewer never contact her
“I used to hear that they heal people with cough at this place, but I was
again. Her brother called the line ten minutes later:
like, ‘how much will I [pay] there?’ but when I heard it was free, that was
“The man who spoke with you earlier is [the patient]’s father. God has what gave me the opportunity to come here” (Patient FGD).
healed [her], she is totally well now. Her father does not want to hear
[from] you or, anyone who talks about DR-TB so, keep off for the sake
3.2.7. Program strengths
of peace.” (Relative to patient not initiated on treatment).
Overwhelmingly, patients cited the free care and financial support
Healthcare workers and program managers also mentioned the lack provided by the program as the major facilitators of access, enabling
of female autonomy to seek care without their husbands’ approval. them to focus on getting better, without the added worries of compen-
sating for lost livelihoods due to the effects of the illness itself and
“Women… of course, you know some women depend on their husbands… workplace stigma. Other strengths of the program were the patient ed-
There are [wives] that [can’t] go out, even when she is sick… and the ucation and counseling sessions.
husband [might] feel like taking her to the hospital is just … maybe On the other hand, healthcare workers mentioned teamwork and
[a] waste [of] time, until the sickness [has made her bedridden].” coordination, pooling of resources from implementing partners, the use
(HCW KII). of technology e.g. WhatsApp messaging within the team to improve
When female patients were asked directly, none of them mentioned patient tracking and GeneXpert results notifications.
that this was a factor. However, one FGD participant mentioned that her “If there are treatment issues, treatment interruption, so that the com-
husband’s persistence was key to her diagnosis. munity based officers [can intervene] immediately and to also respond. If
At the health system level, predominant themes addressed the atti- there are drug reactions you know who to call it could also be the doctor,
tudes, knowledge and skills of providers, which affected linkage and it could be [someone else]. We already have like a coordinated referral
referral to appropriatecare. This was not always negative, as one system and also we use the WhatsApp very well where you just throw [in
participant cited the information given to them by TB officers as any question] and you can be sure there will be a quick response.” (HCW
responsible for changing community perceptions about TB. KII)
“What we heard about TB before the arrival of [the] TB center is that
some wicked people do blow the charm[ed] air … once it is blown at you, 4. Discussion
you contract TB but the arrival of TB officers changed our orientation, …
that it’s not an attack from people but [an] infection” (Community FGD). Our miXed methods analysis of the DR-TB care cascade in Nigeria
Attitudes of healthcare workers, from the perspectives of patients, contributes to the understanding of the main factors influencing access
were predominantly negative before diagnosis. and retention in care for DR-TB patients and brings to bear the impor-
tance of targeting control efforts at different stages of the care cascade.
“When this [illness] started… when I went for [a] test … I was treated Although numbers improved over the period of study, only 2.5% of
anyhow, like sit here, leave here, shouting, and I fought them to stop people with DR-TB successfully navigate the DR-TB care cascade in
chasing me … and embarrassing me” (Patients FGD). Nigeria. The vast majority do not even make it to formal providers. Our
qualitative data suggests there is a lack of awareness regarding TB in
Health workers became much more supportive once patients began
general, and specifically around main symptoms, where and how to
treatment, and this was the same across interviews from different
access free testing, and that TB is curable with appropriate treatment.
centers.
However, there was a 3-fold increase in the ratio of patients who
9
completed treatment, and this was likely due to the scale-up of appro-
evidence from other countries show [55,56]. Data management and
priate DR-TB testing (Gene Xpert). This also translating to improved
correctly tracking patients by verifying contact information is another
numbers at Steps 3–5 of the care cascade - those who got diagnosed,
area that could have cross-cutting impact on the cascade of care [57,58].
treated and completed treatment for DR-TB.
On the health system level, in addition to improving coverage and
Our data sources and design only allow minimal insight into this first
access to GeneXpert testing, our findings suggest that training providers
step, because cohort and interview data were on patients who were
to recognize individuals at risk for DR-TB and on stigma and discrimi-
already diagnosed. However, from what participants recalled, accessing
nation could play a role in reducing the very large gaps 1 and 2 in the
testing was difficult mostly because of a lack of awareness. This resulted
care cascade [59,60]. Additionally, healthcare providers felt under-
in seeking private sector care, including with private hospitals, patent
resourced and unsupported to provide adequate care, agreeing with
medicine stores and traditional healers. Our data suggest that this may
findings in a recent study from India [61].
relate to how people are treated in the public sector or alternative ex-
The significant gaps in accessing testing and diagnostic services
planations about what causes the symptoms. However, some patients
noted in our data agrees with findings on DR-TB cascades in India and
may be lost to follow-up due to poor linkages between the private and
Madagascar, where Gaps 1 and 2 were reportedly the biggest gaps in DR-
the public sector. Respondents mentioned that knowing someone with
TB care [62,63]. These findings are in contrast with the South Africa DR-
knowledge about TB and available services was instrumental in getting
TB care cascade showing treatment initiation and completion were
them into care, similar to studies from South Africa and India [37,38].
the biggest challenges [64].
Interventions to improve program visibility through community
Our findings suggest TB policy implications. Increasing patient
awareness, as suggested by the participants, and engaging the private
awareness of TB symptoms and available services is an important
sector, including with spiritual and traditional healers, have been shown
first step for TB control in Nigeria, since case-finding is reliant on
to dramatically improve TB case finding (up to 100%) in resource-
patients recognizing their symptoms and presenting to a public health
limited settings like Nigeria [39–41].
Our data suggest an estimated thre quarters of DR-TB patients are facility with TB services. This is supported by other studies from Nigeria,
lost at Gap 2 due to misdiagnosis or inadequate provider index of sus- calling for improved public communication around TB [65–67]. Mass
picion, poor provider attitudes, clinic and laboratory challenges and the awareness campaigns have been used sucesfully in South Africa and
poor linkages between the private and public sector. Patients also other settings to create awareness, reduce stigma, and improve case
mentioned fear of prolonged treatment. Provider training and supervi- finding [56,68,69]. Improving accessibility to healthcare facilities with
sion contributed to significant increases in case finding in India and TB testing and treatment could include active case-finding, mobile TB
Ethiopia [40,42]. clinics and working with the private sectors to ensure adequate support
According to the care cascade, the majority of people diagnosed with for referring TB patients for appropriate testing. Interventions might
DR-TB (64%) went on to initiate treatment and 78% of these finished also include behavioural change messages, advocacy with community
treatment. Gaps 3 and 4, treatment enrolment and completion, were leaders and gatekeepers [70]. Improving access to TB care services
sometimes due to individual beliefs and perceptions about healthcare, for women and children need to consider adverse cultural gender and
and fear of treatment, as well as work and family commitments. This parental norms, especially those that could prevent them from accessing
highlights the need to continuously counsel patients, especially on healthcare. Integrating current policies to protect the rights of women
adherence and potential side effects, and to address the opportunity and children to access TB care could potentially improve their health
costs of accessing care, as this has been shown to improve retention in protection [71,72].
care [43]. The financial support given to patients was repeatedly cited as
a major facilitator at this stage and needs to be sustained. 4.1. Comparing different sources of data
Related to treatment completion, patients’ mental health and the toll
from medication side effects were underscored by several respondents. Findings from the quantitative data were generally in agreement
The toXicities of DR-TB medications and their effects on patients’ out- with qualitative findings. Overall, the quantitative findings indicating
comes is widely documented [25,44,45]. The current revision in WHO that males and adults were more likely to progress through the various
guidelines to shorter oral regimens will potentially improve patient steps of the cascade were reflected in the qualitative themes showing
parental and spousal influence impacting access to care and dis-
adherence to treatment, as side effects reduce [46,47]. Several studies
advantaging women and girls, as well as children. Several studies from
have made a case for psychosocial support for DR-TB patients [48–50].
Africa, including Nigeria, and Asia have shown similar barriers to TB
Although DR-TB incidence was higher in adult males, women and
care for women, children and rural dwellers [53,54,73–77].
children faced particular challenges in accessing care due to a lack of
While the data from the 2015 cohort indicated regional differences in
autonomy and adverse gender norms. Our cross-cutting findings of in-
access, we were not able to identify major themes related to this, besides
stances of family members preventing TB care for their family members
the operationalizing of case findings in the different hospital teams,
is not very common in the literature, although some studies have re-
including the use of WhatsApp group messaging. These differences will
ported marriages ending as a result of a TB diagnosis for the woman
need to be further explored.
[51,52]. We found one study in India, where parents prevented their
There were differences between the cohort and the cascade of care
daughter’s TB treatment enrolment to avoid stigma and a cancelled
results with regards to children. The cohort analysis [29] showed chil-
marriage [44]. Other studies from Nigeria have found similar adverse
gender roles impeding access to TB care for women [53,54]. dren were more likely than adults to initiate treatment once
While each level had unique barriers, addressing the cross-cutting diagnosed in the South-West zone, but not at the national-level. One
barriers could serve as a first step for policy change and targeted in- likely reason might be the particular attention given to initiate
terventions. For example, at each level of the cascade, patient beliefs and pediatric patients on treatment once tested within the South-West
perceptions about the symptoms and the path to cure determined zone. This earlier treatment initiation in children might not be a
whether they persisted to treatment completion or not. Patients and complete contradiction as the cascade analysis showed a reduced
providers repeatedly recommended improving community awareness likelihood of progressing from tested to treatment outcome, and not
on TB. This would likely have impact across the continuum of care, as just treatment initiation alone.
1
4.2. Study strengths and limitations

needs to make concerted efforts to improve community awareness about
symptoms and available resources, private sector engagement and
Using qualitative interviewing permitted an in-depth understanding
training of providers, and data management, including patient tracking
of the problem of access from the differing perspectives of individuals
systems.
affected. It is not always the case that the views of patient and their
Gaps in treatment enrolment and completion at the health system
relatives align with those of providers. One strength of this study was
level will require increasing access to services and improved coverage,
that it sought to elicit and compare these different perspectives. In our
especially for remote locations, as well as policies to protect workers in
study, we found that, while health workers mentioned cases where a
need of healthcare. The National TB control program also needs to
lack of female autonomy was a barrier to care, female participants
consider specific approaches to address the barriers faced by children
themselves did not identify this as a problem. This difference in opinions
and women in accessing services.
may have been due to the way the female participants perceived au-
tonomy and cultural norms.
Our study has some limitations. The quantitative data for incidence Funding
and access to testing are estimates using routine data. This may have
introduced bias into cascade gaps because as estimates, they do not COO received funding for field work through the Global Fund New
account for the changing patient populations at each stage of the cascade Funding Model MDRTB Grant (Global Fund to Fight AIDS, Tuberculosis
[8]. The cohort analysis used in the second step links diagnostic to and Malaria: NFM MDRTB Grant), with funds provided through IHVN as
treatment registers and tracks patients to treatment completion. This the Principal Recipient. The funders had no role in study design, data
may have minimized bias in the cascade estimates at the later stages of collection and analysis, decision to publish, or preparationof the
the cascade. manuscript.
Besides 2015, data for the other years used in the cascade estima-
tion and analysis did not show the contribution of the private sector to Ethical Statement
notificaitons and treatment numbers. As a large number of Nigerian TB
patients seek care first in the private sector, this lack of a clear un- The National Health Research Ethics Committee of Nigeria (NHREC/
derstanding of the private sector contribution is a limitation of this 01/01/2007) and the Research Ethics Committee (CER) of the Univer-
analysis. If a significant number of people who first present to the sity of Montreal Hospital (17.060) granted ethical approval for this
private sector are appropriately managed, but not notified to the Na- study. An additional ethical approval was obtained from the Research
tional TB Program, our estimates at various stages may be Ethics Committee (CER) of sciences and health of the University of
overestimated. Montreal (CERSES-19-098-D). All interview participants gave written or
There were other limitations due to its qualitative study design verbal informed consent.
[78]. A large amount and range of interview data made analysis
complex and impossible to present in its entirety. Also, based on the
fact that we conducted interviews in only 2 out of 6 geopolitical zones CRediT authorship contribution statement
in Nigeria, the extent to which our results are generalizable to other
parts of the country is largely unknown. Additionally, given their status Charity Oga-Omenka: Conceptualization, Methodology, Formal
as ‘missing’, we were unable to seek direct feedback from people who analysis, Visualization, Writing - original draft. Jody Boffa: Methodol-
did not present to health centres. Although the perceptions of those ogy, Writing - original draft. Joseph Kuye: Software, Validation,
receiving care provide insight into the reasons for these gaps, we may Writing - review & editing. Patrick Dakum: Resources, Writing - review
have missed potetntial factors that affect the large proportion of losses & editing. Dick Menzies: Methodology, Supervision, Writing - original
at the first stage. draft. Christina Zarowsky: Conceptualization, Methodology, Supervi-
Although participants were further probed and their responses sion, Writing - original draft.
reconfirmed, we cannot exclude the possibility of recall and reporting
biases. We addressed this by triangulating sources, location and Acknowledgements
interview methods. There was an overall consistency in the themes
emerging from the different sources of data. Finally, we did not The authors thank the National TB and Leprosy Control Program
conduct interviews in Northern Nigeria beyond the central geopolitical (NTBLCP) of the Federal Ministry of Health (in Abuja, Plateau and
zone. There is a possibility that particular contexts in these regions OgunState), the International Research Center for EXcellence (IRCE) of
were not explored. the Institute of Human Virology Nigeria(IHVN) for granting access to the
National database and for support in the process of data collection.
5. Conclusion The contents of this publication are solely the responsibility of the
authors and do not necessarily represent the official views of the Global
Our study has shown that, although there is noticeable progress in Fund, NTBLCP or IHVN.
access to DR-TB care in Nigeria between 2013 and 2017, this is not
nearly enough to meet the End TB targets. On average, less than 3% of Appendix
estimated incident cases ever make it to treatment completion. This
presents serious implications for TB control in Nigeria. Major bottle-
necks persist in accessing diagnostic testing and getting diagnosed.
Treatment initiation rates also remain sub-optimal.
To reduce gaps in testing and diagnosis, the National TB program
1
Table A1
C. Oga-Omenka et
The DR-TB care cascade and process indicators (Subbaraman et al., 2019).
Cascade stage Outcome Methods or required 2013 Cases 2014 Cases 2015 Cases [Range] 2016 Cases [Range] 2017 Cases [Range] Process indicators used Methods used for process
indicators for data for outcome [Range] [Range] indicators
cascade steps indicators
Stage 1: Step 1: Number of individuals with incident or prevalent DR-TB in the population Gap 1: Number of individuals with TB who did not reach
Reaching health facilities and access a TB diagnostic test
health
facilities
and
accessing a
TB test
Annual number Population-based TB 590,000 570,000 586,000 407,000 418,000
of individuals prevalence survey [340,000- [340,000- [345,000–890,000] [266,000–579,000] [273,000–594,000]
with incident (2012) 880,000] 870,000]
active TB in a WHO TB Burden
population for Estimate using
all forms of TB extrapolations from
2012 prevalence
survey, yearly
notification data and
expert opinion on case
detection gaps
Estimated Estimation of 17,100 16,500 29,000 20,000 24,000 Time delays in care Qualitative interviews with
number of Incidence of RIF- [9,900–25,500] [9,900–25,200] [15,000–43,000] [12,000–29,000] [14,000–36,000] seekingIndividuals who individuals starting DR-TB
individuals with resistance in the died of TB without treatment at health facilities and
DR-TB annual tuberculosis having received DR-TB communitiesQualitative
burden care interviews with families of
individuals who died of probable
DR-TB
1
Qualitative interviews with

providers of DR-TB care at the
health center and community
levels
Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020)

Stage 2: Step 2: Number of individuals with DR-TB who reached health facilities and accessed a TB diagnostic test Gap 2: Number of individuals with TB who accessed a TB
Diagnosis diagnostic test but did not get successfully diagnosed
Number of EXtrapolation from 3700 3300 4700 5200 5400 Health system–related In-depth interviews with patients
individuals with WHO TB burden [2,800–4,600] [2,500–4,200] [3700–5700] [4100–6200] [4200–6500] delays in diagnosis starting DR-TB treatment and
DR- TB who estimating the their supporters
accessed TB tests proportion of DR-TB Qualitative interviews with
among new and providers of DR-TB diagnosis and
previously treated treatment at the health center
patients among and community levels
notified pulmonary TB
cases
(4.3% [3.2–5.4] of new
cases, 25%
[19–24,26–32] of
previously treated)
Stage 3: Step 3: Number of individuals diagnosed with DR-TB Gap 3: Number of individuals diagnosed with TB who did
Linkage to not get registered in treatment
treatment
Number of Identified through 669 798 996 1691 2300 Delays in treatment In-depth interviews with patients
individuals with National Gene Xpert initiation starting DR-TB treatment and
DR TB who were register (GX Alert) their supporters
successfully Qualitative interviews with
diagnosed as providers of DR-TB diagnosis and
(continued on next page
References
die, or are lost to follow-on DR-TB treatment and their up

TB treatment (due to treatment failure, loss to follow-
reasons for patients whoIn-depth interviews with patients
providers of DR-TB diagnosis

and treatment at the health
[1] WHO. No Time to Wait: Securing the future from drug-resistant infections - Report
Gap 4: Number of individuals who did not complete

treatment at the health to the Secretary-General of the United Nations. 2019.
center and community
and community levels

[2] Madhu Pai. Drug-Resistant TB: A Clear And Present Danger. Forbes. 2019 May
Gap 5: Number of individuals who experienced

continuation phases ofQualitative interviews with
2019.
process indicators
Methods used for
[3] WHO. Global tuberculosis report 2019. 2019.
post- treatment TB recurrence or death

[4] Gupta-Wright A, Tomlinson GS, Rangaka MX, Fletcher HA. World TB Day The
TB treatment
Challenge of Drug Resistant Tuberculosis. F1000Research 2018 2018;7.
[5] Onyedum CC, Alobu I, Ukwaja KN. Prevalence of drug-resistant tuberculosis in
levels
Nigeria: a systematic review and meta-analysis. PLoS One 2017;12(7).
in the intensive andsupporters

[6] Gehre F, Otu J, Kendall L, Forson A, Kwara A, Kudzawu S, et al. The emerging
threat of pre-extensively drug-resistant tuberculosis in West Africa: preparing for
large-scale tuberculosis research and drug resistance surveillance. BMC Med 2016;
14(1):160.
[7] NBLCP/FMOH. First National TB Prevalence Survey Nigeria. Nigeria: National
Process indicators
Tuberculosis & Leprosy Control Program, Federal Ministry of Health Health. DoP;
2012.
Proportion of
[8] Subbaraman R, Nathavitharana RR, Mayer KH, Satyanarayana S, Chadha VK,

Arinaminpathy N, et al. Constructing care cascades for active tuberculosis: a
strategy for program monitoring and identifying gaps in quality of care. PLoS Med
ther
2019;16(2):e1002754.
[9] NBS. DEMOGRAPHIC STATISTICS BULLETIN 2017. Abuja, Nigeria: National
Bureau of Statistics Nigeria, Division DS; 2017 November 2016.
[10] National Bureau of Statistics. DEMOGRAPHIC STATISTICS BULLETIN 2015. Abuja,
Nigeria: National Bureau of Statistics Nigeria, Division DS; 2016 November 2016.
[11] Makinde OA, Sule A, Ayankogbe O, Boone D. Distribution of health facilities in
2017 Cases
Nigeria: implications and options for universal health coverage. Int J Health Plann
Manage 2018;33(4):e1179–92.
[12] PharmAccess. A Closer Look at the Healthcare System in Nigeria. In: PharmAccess,
17
editor. 2016.
[13] Organization WH. Engaging private health care providers in TB care and
prevention: a landscape analysis. World Health Organization; 2018.
[14] Ukwaja KN, Alobu I, Nweke CO, Onyenwe EC. Healthcare-seeking behavior,
treatment delays and its determinants among pulmonary tuberculosis patients in
2016 Cases
rural Nigeria: a cross-sectional study. BMC Health Serv Res 2013;13(1):25.

[15] Gidado M, Onazi O, Obasanya O, Chukwueme N, Onazi M, Omoniyi A, et al.
Assessing the effectiveness of Xpert MTB/RIF in the diagnoses of TB among HIV
12
smear negative TB patients in Nigeria. J Health Sci 2014;2:145–51.

9
[16] Tope AT. Can Nigeria sustain the fight against drug resistant mycobacterium
tuberculosis? J Microbiol Res 2014;4(2):72–7.
[17] NBLCP/FMOH. The National Strategic Plan for Tuberculosis Control: Towards
Universal Access to Prevention, Diagnosis and Treatment- 2015-2020. Nigeria:
2015 Cases
National Tuberculosis & Leprosy Control Program, Federal Ministry of Health

Health. DoP; 2014 August 2014.
[18] NBLCP/FMOH. 2015 Annual Report National Tuberculosis and Leprosy Control
Programme. Nigeria: National Tuberculosis & Leprosy Control Program, Federal
6
Ministry of Health Health. DoP; 2015 August 2014.

[19] Cazabon D, Suresh A, Oghor C, Qin ZZ, Kik SV, Denkinger CM, et al.
Implementation of Xpert MTB/RIF in 22 high tuberculosis burden countries: are
we making progress? Eur Respir J 2017;50(2).
[20] WHO. Global tuberculosis report 2016. 2016.
[21] WHO. Global tuberculosis report 2017: World Health Organization; 2017.
Cases
2014
4
[25] Meressa D, Hurtado RM, Andrews JR, Diro E, Abato K, Daniel T, et al. Achieving
high treatment success for multidrug-resistant TB in Africa: initiation and scale-up
of MDR TB care in Ethiopia—an observational cohort study. Thorax 2015;70(12):
Step 5: Number of individuals who completed DR-TB
1181–8.
Step 4: Number of individuals registered in DR-TB
Cases
2013
[26] Hong QN, Fa`bregues S, Bartlett G, Boardman F, Cargo M, Dagenais P, et al.

3
The MiXed Methods Appraisal Tool (MMAT) version 2018 for information
professionals and researchers. Educ Inf 2018;34(4):285–91.
[27] Creswell JW, Clark VP, Garrett A. Advanced miXed methods research. Handbook of
miXed methods in social and behavioural research. Thousand Oaks, CA: Sage;
TB electronic DR-
TB electronic DR-
required data for
2003. p. 209–40.
[28] Glaziou P, Sismanidis C, Zignol M, Floyd K. Methods used by WHO to estimate the
register (e-TB
TB treatment
registered on(e-TB Manager) DR-
Methods or
global burden of TB disease. Geneva: Global TB Programme, WHO; 2016.

treatment
outcome
[29] Oga-Omenka C, Zarowsky C, Agbaje A, Kuye J, Menzies D. Rates and timeliness of

treatment initiation among drug-resistant tuberculosis patients in Nigeria-a
retrospective cohort study. PLoS One 2019;14(4). e0215542-e.
[30] Haber N, Pillay D, Porter K, Ba¨rnighausen T. Constructing the cascade of HIV
care: methods for measurement. Curr Opin HIV AIDS 2016;11(1):102–8.
[31] Gale NK, Heath G, Cameron E, Rashid S, Redwood S. Using the framework method
TB treatment
for the analysis of qualitative data in multi-disciplinary health research. BMC Med
resistant TB
indicators
Res Method 2013;13(1):117.

Outcome
individu
Number
patients
cascade
Numbe
[32] Oga-Omenka C, Tseja-Akinrin A, Sen P, Mac-Seing M, Agbaje A, Menzies D, et al.

steps
who
Factors influencing diagnosis and treatment initiation for multidrug-resistant/

for
of
rifampicin-resistant tuberculosis in siX sub-Saharan African countries: a miXed-

methods systematic review. BMJ Global Health 2020;5(7):e002280.
[33] NTBLCP/FMOH. DR-TB Program Data. [Program data]. 2015.
[34] NBLCP/FMOH. GXAlert Gene Xpert Database. Nigeria: National Tuberculosis &
Retenti
treatm
treatm
Stage 4:
Stage 5:
Table A1
Cascade
Post-
on in
Leprosy Control Program, Federal Ministry of Health Health. DoP; 2015 August
ent
2014.
[35] NBLCP/FMOH. e-TB Manager Treatment Database. Nigeria: National Tuberculosis
& Leprosy Control Program, Federal Ministry of Health Health. DoP; 2015 2017.
1
[36] Global health observatory (GHO) data. 2020 [Internet]. 2020. Available from: http follow-up from antiretroviral treatment in Lilongwe, Malawi. BMC Infect Dis 2011;
s://www.who.int/data/gho/indicator-metadata-registry/imr-details/1364. 11(1):31.
[37] Naidoo P, Van Niekerk M, Du Toit E, Beyers N, Leon N. Pathways to multidrug- [58] Stalin P, Manikandan M, Antony V, Murugan N, Singh Z, Kisku KH, et al.
resistant tuberculosis diagnosis and treatment initiation: a qualitative comparison Identifying and addressing factors contributing to pretreatment loss to follow-up
of patients’ experiences in the era of rapid molecular diagnostic tests. BMC Health of tuberculosis patients referred for treatment from medical colleges in
Serv Res 2015;15(1):488. Pondicherry: an implementation research. Indian J Commun Med
[38] Yadav SK, Damor R, Kantharia S, Tiwari M. Assessment of knowledge and 2020;45(1):27.
treatment seeking behaviour among tuberculosis and multi-drug resistant [59] Karamagi E, Sensalire S, Muhire M, Kisamba H, Byabagambi J, Rahimzai M, et al.
tuberculosis patients:-a case control study. IOSR J Dent Med Sci 2015;14(7):66– Improving TB case notification in northern Uganda: evidence of a quality
71. improvement-guided active case finding intervention. BMC Health Services Res
[39] Sharma N, Taneja D, Pagare D, Saha R, Vashist R, Ingle G. The impact of an IEC 2018;18(1):1–12.
campaign on tuberculosis awareness and health seeking behaviour in Delhi, India. [60] Wu S, Roychowdhury I, Khan M. Evaluating the impact of healthcare provider
Int J Tuberc Lung Dis 2005;9(11):1259–65. training to improve tuberculosis management: a systematic review of methods
[40] Yassin MA, Datiko DG, Tulloch O, Markos P, Aschalew M, Shargie EB, et al. and outcome indicators used. Int J Infect Dis 2017;56:105–10.
Innovative community-based approaches doubled tuberculosis case notification [61] Thomas BE, Suresh C, Lavanya J, Lindsley MM, Galivanche AT, Sellappan S, et
and improve treatment outcome in Southern Ethiopia. PLoS One 2013;8(5). al. Understanding pretreatment loss to follow-up of tuberculosis patients: an
[41] Colvin C, Mugyabuso J, Munuo G, Lyimo J, Oren E, Mkomwa Z, et al. Evaluation explanatory qualitative study in Chennai, India. BMJ Global Health 2020;5(2):
of community-based interventions to improve TB case detection in a rural district e001974.
of Tanzania. Global Health: Sci Pract 2014;2(2):219–25. [62] Knoblauch AM, Lapierre SG, Randriamanana D, Raherison MS, Rakotoson A,
[42] Ambe G, Lo¨nnroth K, Dholakia Y, CopreauX J, Zignol M, Borremans N, et al. Raholijaona BS, et al. Multidrug-resistant tuberculosis surveillance and cascade of
Every provider counts: effect of a comprehensive public-private miX approach for care in Madagascar: a five-year (2012–2017) retrospective study. BMC Med 2020;
TB control in a large metropolitan area in India. Int J Tuberc Lung Dis 18(1):1–14.
2005;9(5): 562–8. [63] Subbaraman R, Nathavitharana RR, Satyanarayana S, Pai M, Thomas BE,
[43] Law S, Daftary A, O’Donnell M, Padayatchi N, Calzavara L, Menzies D. Chadha VK, et al. The tuberculosis cascade of care in India’s public sector: a
Interventions to improve retention-in-care and treatment adherence among systematic review and meta-analysis. PLoS Med 2016;13(10):e1002149.
patients with drug-resistant tuberculosis: a systematic review. Eur Respir J [64] Naidoo P, Theron G, Rangaka MX, Chihota VN, Vaughan L, Brey ZO, et al. The
2019;53 (1). South African tuberculosis care cascade: estimated losses and methodological
[44] Deshmukh RD, Dhande D, Sachdeva KS, Sreenivas A, Kumar A, Satyanarayana S, challenges. J Infect Dis 2017;216(suppl_7). S702–S13.
et al. Patient and provider reported reasons for lost to follow up in MDRTB [65] Hassan A, Olukolade R, Ogbuji Q, Afolabi S, Okwuonye L, Kusimo O, et al.
treatment: a qualitative study from a drug resistant TB Centre in India. PLoS One Knowledge about tuberculosis: a precursor to effective TB control—findings from
2015;10(8). a follow-up national KAP study on tuberculosis among Nigerians. Tuberculosis
[45] Awofeso N. Anti-tuberculosis medication side-effects constitute major factor for Res Treatment 2017;2017.
poor adherence to tuberculosis treatment. Bulletin of the World health [66] Jombo G, Mbaave PT. Global tuberculosis burden: is Nigeria losing the
Organization; 2008. p. 86. B-D. war? J BioMed Res Clin Pract 2018;1(1):iX–Xi.
[46] Abidi S, Achar J, Neino MMA, Bang D, Benedetti A, Brode S, et al. Standardised [67] Babatunde OI, Bismark EC, Amaechi NE, Gabriel EI, Olanike A-UR. Determinants of
shorter regimens versus individualised longer regimens for rifampin-or treatment delays among pulmonary tuberculosis patients in Enugu Metropolis,
multidrug- resistant tuberculosis. Eur Respir J 2020;55(3). South-East, Nigeria. Health 2015;7(11):1506.
[47] WHO. Rapid Communication: Key changes to the treatment of drug-resistant [68] Golub JE, Mohan C, Comstock G, Chaisson RE. Active case finding of
tuberculosis. World Health Organization: Geneva, Switzerland. 2019. tuberculosis: historical perspective and future prospects. Int J Tuberc Lung Dis
[48] Thomas BE, Shanmugam P, Malaisamy M, Ovung S, Suresh C, Subbaraman R, et al. 2005;9(11): 1183–203.
Psycho-socio-economic issues challenging multidrug resistant tuberculosis [69] Meiring C, van Helden PD, Goosen WJ. TB control in humans and animals in South
patients: a systematic review. PLoS One 2016;11(1). Africa: a perspective on problems and successes. Front Veterinary Sci 2018;5:298.
[49] Khanal S, Elsey H, King R, Baral SC, Bhatta BR, Newell JN. Development of a [70] Oshi D, Chukwu J, Nwafor C, Chukwu NE, Meka AO, Anyim M, et al. Support and
patient-centred, psychosocial support intervention for multi-drug-resistant unmet needs of patients undergoing multidrug-resistant tuberculosis (MDR-TB)
tuberculosis (MDR-TB) care in Nepal. PLoS One 2017;12(1). treatment in southern Nigeria. Int J Health Plann Manage 2019.
[50] Kaliakbarova G, Pak S, Zhaksylykova N, Raimova G, Temerbekova B, Hof S. [71] Federal Ministry of Health NU. Women and children rights in Nigeria: A wake up
Psychosocial support improves treatment adherence among MDR-TB patients: call - Situation assessment and analysis. . Abuja, Nigeria; 2002.
experience from East Kazakhstan. Open Infect Dis J 2013;7(1). [72] Kura SM, Yero BU. An analysis of gender inequality and national gender policy in
[51] Sharma R, Yadav R, Sharma M, Saini V, Koushal V. Quality of life of multi drug Nigeria. Int J Sci Eng Res 2013;4(1):1–23.
resistant tuberculosis patients: a study of north India. Acta Med Iranica 2014: [73] Karim F, Islam MA, Chowdhury A, Johansson E, Diwan VK. Gender differences in
448–53. delays in diagnosis and treatment of tuberculosis. Health Policy Plann 2007;22(5):
[52] Onifade DA, Bayer AM, Montoya R, Haro M, Alva J, Franco J, et al. Gender- 329–34.
related factors influencing tuberculosis control in shantytowns: a qualitative [74] Okeibunor J, Onyeneho N, Chukwu J, Post E. Where do tuberculosis patients go for
study. BMC Public Health 2010;10(1):381. treatment before reporting to DOTS clinics in southern Nigeria. Tanzania J Health
[53] Ibrahim LM, Hadejia IS, Nguku P, Dankoli R, Waziri NE, Akhimien MO, et al. Res 2007;9(2):94–101.
Factors associated with interruption of treatment among Pulmonary Tuberculosis [75] Tarimo GB. Delay in seeking care among tuberculosis patients attending
patients in Plateau State, Nigeria. 2011. Pan Afr Med J 2014;17(1). tuberculosis clinics in Rungwe district. Tanzania: Muhimbili University of Health
[54] Oshi DC, Oshi SN, Alobu IN, Ukwaja KN. Gender-related factors influencing and Allied Sciences; 2012.
women’s health seeking for tuberculosis care in Ebonyi State, Nigeria. J Biosoc Sci [76] Sullivan BJ, Esmaili BE, Cunningham CK. Barriers to initiating tuberculosis
2016;48(1):37–50. treatment in sub-Saharan Africa: a systematic review focused on children and
[55] Datiko DG, Lindtjørn B. Health extension workers improve tuberculosis case youth. Global health Action 2017;10(1):1290317.
detection and treatment success in southern Ethiopia: a community randomized [77] Yang W-T, Gounder CR, Akande T, De Neve J-W, McIntire KN, Chandrasekhar A,
trial. PLoS One 2009;4(5):e5443. et al. Barriers and delays in tuberculosis diagnosis and treatment services: does
[56] Islam Z, Sanin KI, Ahmed T. Improving case detection of tuberculosis among gender matter? Tuberculosis Res Treatment 2014;2014.
children in Bangladesh: lessons learned through an implementation research. BMC [78] Hodkinson P, Hodkinson H, (eds.). The strengths and limitations of case study
public health. 2017;17(1):131. research. learning and skills development agency conference at Cambridge; 2001.
[57] Weigel R, Hochgesang M, Brinkhof MW, Hosseinipour MC, BoXshall M, Mhango E,
et al. Outcomes and associated risk factors of patients traced after being lost to
1
Update
Journal of Clinical Tuberculosis and Other Mycobacterial Diseases
Volume 24, Issue , August 2021, Page
DOI: https://doi.org/10.1016/j.jctube.2021.100242
Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 24 (2021) 100242
Contents lists available at
Journal of Clinical Tuberculosis and Other

Mycobacterial Diseases
journal homepage:
Erratum regarding previously published articles
The Declaration of Competing Interest statements were not

included in the published version of articles that appeared in the Academy EXperience (Volume 20C, August 2020).
Volumes 20 and Clinical efficacy of Vitamin D supplementation on pulmonary TB
21 of the Journal of Clinical Tuberculosis and Other Mycobacterial patients: the evidence of clinical trials (Volume 20C, August 2020).
Diseases. For the below articles, the authors declare that they have no Understanding the Gaps in DR-TB Care Cascade in Nigeria: a
known competing financial interests or personal relationships that could sequential miXed-method study (Volume 21C, December 2020).
have appeared to influence the work reported in this paper. TB and COVID - Public and private health sectors adapt to a new
Validity of a CB-NAAT assay in diagnosing Tuberculosis in compar- reality (Volume 21C, December 2020).
ison to culture: A study from an urban area of South India (Volume Quantitative structure-activity relationship (QSAR) and molecular
21C, December 2020). docking of Xanthone derivatives as anti-tuberculosis agents (Volume
Real-world treatment patterns in patients with nontuberculous 21C, December 2020).
mycobacterial lung disease (Volume 20C, August 2020). Genexpert assay – A cutting-edge tool for rapid tissue diagnosis of
Quality Improvement and Healthcare: The Mayo Clinic Quality tuberculous lymphadenitis (Volume 21C, December 2020).
DOIs of original article: https://doi.org/10.1016/j.jctube.2020.100178, https://doi.org/10.1016/j.jctube.2020.100193,

https://doi.org/10.1016/j.jctube.2020. 100199, https://doi.org/10.1016/j.jctube.2020.100170, https://doi.org/10.1016/j.jctube.2020.100174,
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i An update to this article is included at the end

Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020) 100193

Contents lists available at

Journal of Clinical Tuberculosis and Other

Understanding the gaps in DR-TB care cascade in Nigeria: A sequential

Available online 9 October 2020

2. Methodology Our sequential miXed-methods study (Fig. 1) utilised the following

Fig. 1. MiXed-methods sampling strategy.

Fig. 2. Trends in DR-TB Care Cascade in Nigeria 2013–2017.

Fig. 3. Average Retention and Losses in DR-TB Care Cascade in Nigeria.

TOTAL n (%) n (%) n (%) n (%) n (%) OR [95% CI]

29,000 4700 996 660 511

Fig. 4. Summary factors influencing DR-TB care cascade.

3.2.3. Gap 2: from testing to diagnosis

The major cross-cutting themes on interpersonal influences were

4.2. Study strengths and limitations

Qualitative interviews with

Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020)

die, or are lost to follow-on DR-TB treatment and their up

reasons for patients whoIn-depth interviews with patients

providers of DR-TB diagnosis

Gap 4: Number of individuals who did not complete

and community levels

Gap 5: Number of individuals who experienced

[3] WHO. Global tuberculosis report 2019. 2019.

post- treatment TB recurrence or death

Nigeria: a systematic review and meta-analysis. PLoS One 2017;12(7).

in the intensive andsupporters

[8] Subbaraman R, Nathavitharana RR, Mayer KH, Satyanarayana S, Chadha VK,

rural Nigeria: a cross-sectional study. BMC Health Serv Res 2013;13(1):25.

smear negative TB patients in Nigeria. J Health Sci 2014;2:145–51.

National Tuberculosis & Leprosy Control Program, Federal Ministry of Health

Ministry of Health Health. DoP; 2015 August 2014.

[26] Hong QN, Fa`bregues S, Bartlett G, Boardman F, Cargo M, Dagenais P, et al.

global burden of TB disease. Geneva: Global TB Programme, WHO; 2016.

[29] Oga-Omenka C, Zarowsky C, Agbaje A, Kuye J, Menzies D. Rates and timeliness of

Res Method 2013;13(1):117.

[32] Oga-Omenka C, Tseja-Akinrin A, Sen P, Mac-Seing M, Agbaje A, Menzies D, et al.

Factors influencing diagnosis and treatment initiation for multidrug-resistant/

rifampicin-resistant tuberculosis in siX sub-Saharan African countries: a miXed-

Contents lists available at

Journal of Clinical Tuberculosis and Other

Erratum regarding previously published articles

The Declaration of Competing Interest statements were not

DOIs of original article: https://doi.org/10.1016/j.jctube.2020.100178, https://doi.org/10.1016/j.jctube.2020.100193,

Available online 6 May 2021

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