Understanding The Gaps in DR TB Care Casc - 2020 - Journal of Clinical Tuberculo

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 ScienceDirect
Journal of Clinical Tuberculosis and Other

Mycobacterial Diseases
journal homepage: www.elsevier.com/locate/jctube
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 (ÉSPUM), 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: Background: Despite the availability of free drug-resistant tuberculosis (DR-TB) care in Nigeria since 2011, the
TB Care Cascade country continues to tackle low case notification and treatment rates. In 2018, 11% of an estimated 21,000 cases
Nigeria were diagnosed and 9% placed on treatment. These low rates are nevertheless a marked improvement from 2015
Access to healthcare
when only 3.4% were diagnosed and 2.3% placed on treatment of an estimated 29,000 cases. This study de
Drug-resistant tuberculosis
scribes the Nigerian DR-TB care cascade from 2013 to 2017 and considers factors influencing gaps in care.
Mixed-methods
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 al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 21 (2020) 100193
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
ditions and fever [13,14]. Patients, after onset of symptoms, visited
Rifampicin- or multidrug-resistant tuberculosis (DR-TB) actively PMVs (79%), traditional healers (10%), and private hospitals (10%)
infected an estimated 484,000 people and took 214,000 lives in 2018, [14]. Despite this, only 11% of total TB notifications come from the
threatening to reverse years of advances in global TB prevention and private sector, or less than 3% of estimated incidence [13].
control [1–3]. Drug resistance is an ongoing challenge, especially in Nigeria adopted the use of GeneXpert MTB/RIF (Xpert) technology
settings where healthcare systems are fragmented, suggesting gaps in in 2011 in several national reference laboratories, increasing access to
the care cascade [3,4]. DR-TB diagnosis [15,16]. Prior to this, diagnosis for TB relied mostly on
Nigeria accounts for 4% of the global DR-TB burden and 27% of the smear microscopy, culture, molecular line probe assay and drug sus
incidence in Africa [3]. While the World Health Organization (WHO) ceptibility testing [7,17]. Initially, GeneXpert use was reserved for
estimates that 4.3% of new and 15% of previously-treated people with testing HIV patients, presumed DR-TB cases, children, and extra pul
TB in Nigeria have drug-resistant TB [3], others have suggested that the monary TB cases [18,19]. Treatment for DR-TB patients began with a
incident rate of DR-TB is much higher [5,6]. In a meta-analysis of 8,002 hospital-based model in 2010 and evolved to include community-based
adult TB patients from across the country, Onyedum et al found 32% of DR-TB treatment initiation in 2013 [15,17]. By the end of 2015, the
new (734/2892) and 53% of previously treated people (1467/5020) had country had scaled GeneXpert testing to 201 sites, from 7 sites in 2011,
DR-TB [5]. Gehre et al found 32% (9/28) and 66% (58/88) respectively expanded testing algorithms to include all presumed TB cases, imple
in Lagos state [6]. mented DR-TB treatment in facilities within 16 States and community
Furthermore, Nigeria has particularly low notification and treatment DR-TB initiation in 27 States, with support from the Global Fund and
rates of DR-TB. WHO estimates that only 11% of people with DR-TB other partners [17,18]. At the end of 2015, 12% of Gene Xpert sites and
were diagnosed and 9% placed on treatment in 2018, compared to the 16% of DR-TB hospital bedspaces were in 3 privately owned facilities
39% diagnosis and 32% treatment rates globally [3]. The 2012 Nigerian [18].
National Survey found 75% of smear-positive cases presented with TB
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 2.2. Study design and methods
care providers in Nigeria.
Our sequential mixed-methods study (Fig. 1) utilised the following
2. Methodology methods: a review of Nigeria’s DR-TB cascade over 2013–2017 using
data from WHO Global TB Reports [20–24], a cohort analysis of patients
2.1. Study setting diagnosed in 2015, and a qualitative study based on semi-structured
individual interviews with a purposive sample of respondents. We
2.1.1. National and TB program context used the Mixed Methods Appraisal Tool (MMAT) [25] to conceptualize,
Nigeria, with an estimated 193 million people in 2016 [9], has 36 develop and interpret findings from this study [26].
States and one Federal Capital Territory, across 6 geopolitical zones: The purpose of this sequential transformative mixed methods study
North-Central, North-East, North-West, South-East, South-South and [27] was to understand the health system and patient barriers and fa
South-West [10]. In 2016, there were an estimated 34,140 health fa cilitators to the DR-TB care cascade. The quantitative phase explored
cilities in Nigeria- with 88% of them primary, 11% secondary and 0.13% health system and patient factors associated with gaps in the DR-TB care
tertiary [11,12]. Of these, 67% were public-funded and 33% private continuum. The qualitative phase enhanced the understanding of the
sector health facilities, excluding patent medicine vendors (PMVs) and health system and patient-related factors for these gaps.
private pharmacies [11]. In terms of geopolitical distribution of health
facilities, the North-East had 18.6, North-West 14.4, North-Central had 2.3. Quantitative data collection and analysis
25.8, South-West 20.4, South-East 23.4 and South-South 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 Our second approach is cohort-based, and is a denominator-
data from DR-TB in the national treatment register, allowing for further denominator linked method [8,30]. Recurrence-free survival was also
insights on gaps in care revealed across the 5 years. The primary results 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 (GxAlert) 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 vassarstats.net) to perform descriptive statistics and tests for associa
drug-resistant TB, 4) Number of individuals registered on DR-TB treat tion. We used Pearson’s chi-squared test to determine associations and
ment and 5) Number of patients who completed TB treatment. Fisher’s exact test to compare differences between categorical variables.
Recurrence-free survival, the final step of the TB care cascade, was not
included as there was insufficient data to measure this. Unlike other 2.4. Qualitative data collection and analysis
years, DR-TB incident cases for Nigeria were not explicitly stated in the
WHO annual reports for 2013 and 2014 [23,24]. Rather, we calculated Our qualitative study involved interviews of patients, relatives, and
DR-TB incidence based on the 2.9% of new TB events estimated by the providers in Ogun and Plateau states, as well as program managers in
WHO for these years. National program data is disaggregated for age, Benue and Abuja, the Federal Capital Territory (FCT). A total of 57 in
sex and geopolitical zone. We used notification data to describe the same terviews were conducted in these States, including 10 focus group dis
for incidence and testing access [18]. The outcome indicators, including 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 3. Results
and strengths, as well as their perception of access barriers and facili
tators. Patients and their treatment supporters were asked to describe 3.1. Quantitative results
barriers and facilitators to accessing DR-TB care that they, their relative
or someone they knew had experienced. Community interviews 3.1.1. Changes in DR-TB care cascade in Nigeria, 2013–2017
explored common beliefs and practices around TB among the general Our data shows an gradual increase in numbers retained across all
population. We grouped themes into the different stages of DR-TB care stages of the cascade between 2013 and 2017. Graphs showing each
based on participants description of barriers and facilitators they faced stage of the DR-TB care cascade from 2013 to 2017 are described in
as they navigated the care process, although they were not specifically more detail below.
asked to match these factors to all the stages. Estimated incidence varied between 2013 and 2017 due to differ
Government and program managers at the central level were asked ences in measurements (Appendix 1). According to the WHO, Nigeria
about national policies and resources available for DR-TB control and DR-TB incidence estimates fell from 29,000 in 2015 to 20,000 in 2016 (a
how these resources were distributed nationally and within each State. reduction of 32%) when data on the prevalence of HIV among prevalent
They were also asked about the strengths and challenges within the TB cases derived from the 2012 national prevalence surveys from
program and how these might have affected different groups of patients. Nigeria was used to re-estimate TB incidence ([21], p.24). We have
All interviews were conducted between September and November elected to use a 5-year average of estimated incidence.
2017 by CO, using interview guides developed by the research team and The increases in cases diagnosed and treated over the 5 years was
piloted at the beginning of the data collection. Initial entry meetings statistically significant (p < 0.0001) (Fig. 2). In step 5, treatment success
were held with national and state coordinators, as well as clinic man rate stayed relatively the same from 76.9% in 2013 to 76.7% in 2016.
agers at both treatment meetings to discuss overall objectives of the Data were unavailable on the number of patients diagnosed in 2017 who
research and sampling strategies. Participants were selected based on completed treatment.
their role in the DR-TB program and availability during the interview Percentage retained, which is the ratio between patients who
timeframe. Informed consents were written or verbally acknowledged completed treatment and the estimated incidence for the year, increased
before each interview. All interviews with patients were conducted from 1.5% to 4.8% between 2013 and 2016, representing a 3-fold
outdoors in the treatment centers with patients who had been on increase.
treatment for more than two weeks. Interviews were conducted in En The percentage losses between each stage of care are shown in Fig. 3.
glish and respondents were encouraged to respond in or ask for trans On average, between 2013 and 2016, 80% of estimated DR-TB patients
lation into Nigerian pidgin, Yoruba or Hausa as needed. Interviews were did not gain access to testing for TB or drug susceptibility. Three-
audio-recorded and transcribed. There were instances of responses quarters of those who were tested were never diagnosed. Of those
translated from the Yoruba language, the predominant language in the diagnosed, 35% were not initiated on treated, and 23% of those treated
South West of Nigeria and pidgin English by translators fluent in those did not complete treatment. The biggest losses over these years were in
languages. Transcripts were sent back to 17 participants who had earlier testing and diagnosis access, as more than 60% of those diagnosed were
agreed to be contacted for accuracy checking. Six participants respon treated, and went on to complete their treatment.
ded, with 2 requesting minor revisions, and transcripts were revised
accordingly prior to analysis. 3.1.2. Characteristics of patients within the DR-TB care cascade in 2015
We used a framework approach involving both inductive and Data sources for the cascade steps and gaps for patients diagnosed in
deductive thematic analysis [31]. Codes were inductively derived and 2015 are shown in Table 1.
assigned to new themes or deductively derived from themes identified The DR-TB diagnosis and treatment data for 2015, disaggregated by
from an initial systematic review of barriers and facilitators to DR-TB age, sex and geopolitical location, gives a closer look into the gaps in
care [32]. Interviews were coded by the first author (CO) with the care (Table 2). Among the 29,000 people estimated to have to TB of any
help of 2 assistants. All themes and codes were double-checked by CO. form in 2015, 4700 were estimated as DR-TB cases among notified
Other members of the research team checked the thematic analysis for pulmonary TB cases. The WHO estimates these as the DR-TB patients
overall alignment with study objectives. Transcripts were coded with aid expected to be found among all notified pulmonary TB patients for a
of Quirkos software, version 1.6.1. given year, if all notified pulmonary TB patients were tested for RIF-
The research team comprised two senior scientists (CZ and DM) with resistance using WHO-recommended diagnostic tests [36]. This is
extensive experience in social, implementation science and TB research; different from the absolute number of patients tested for DR-TB (with or
a PhD researcher (CO) and post-doctoral fellow (JB) with over 15 years without a positive result) in the year. Subbaraman et al, 2019 [8]
of combined implementation and mixed-methods research experience in (Table 1) recommends using this estimate of DR-TB among notified
HIV/AIDS and TB in sub-Saharan Africa; a DR-TB National program pulmonary TB cases as a proxy for the total number of DR-TB patients
manager (JK), implementing partner and seasoned researcher in Nigeria who likely accessed testing during the same period. Of these, 996 were
(PD); and a research assistant who was a recent science graduate fluent diagnosed with DR-TB, 660 were treated and 511 completed treatment.
in Yoruba and the pidgin English widely spoken in Nigeria. The research The association between age, sex and geopolitical zone and pro
assistant was trained for 2 weeks on qualitative interview skills before gression through the cascade of care was shown to be statistically sig
fieldwork. None of the researchers were directly involved in patient nificant. Using the Fisher’s exact probability test, children had lower
management for DR-TB. odds than adults (0.3, 95% CI 0.1–0.7), males had 1.34 (95% CI 1.0–1.7)
greater odds than females, and patients in the north had lower odds than
2.5. Ethics those in the south (0.4, 95% CI 0.3–0.5) to move from diagnosis to
treatment completion. A further analysis of this cohort are presented in a
The National Health Research Ethics Committee of Nigeria (NHREC/ 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 facilities individuals who died of probable DR-TB•
resistance survey (2010)• National TB and access a TB diagnostic test Pathways of individuals on DR-TB treatment•
prevalence survey (2012) [7]• NTP program 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 test individuals who died of probable DR-TB•
(reached TB reference laboratory data• NTP case 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 [35]• 660 [–] 4: Number of individuals who did • Community members of individuals who did
treatment 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 community
follow-up, or death) levels
5. Treatment • National e-TB (treatment) database [35]• 511 [–] 5: 5: Number of individuals who No data
completed WHO [20] experienced post-treatment TB
recurrence or death
Table 2
Characteristics of patients within each stage of the care cascade in 2015.
Characteristic *Estimated *Estimated Diagnosed Treated Completed Pearson X2 p- Diagnosed Vs Completed Fisher’s
Incidence Tested value exact test
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 influencing For many, initial care seeking involved alternatives to the public
each stage of the care cascade into individual/patient factors, interper sector. For example, many patients or their loved ones described first
sonal influences operating at the family or community level, and finally seeking care through “prayer houses,” traditional healers, or through the
at the health system level. We present several examples, especially for private sector:
testing and diagnostic gaps, which were identified as the major barriers “[When this illness started], I went to private hospitals, and they did not
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 straight for
3.2.2. Gap 1: accessing to TB diagnostics ward, they did not answer me. I started using different types of herbal
Many respondents described individual delays in accessing testing. mixture for like one month but I had gone round earlier before I got here.”
Predominantly, this related to a number of uncertainties about TB and to (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 know
When asked what could have helped them or their loved one get that this TB has to be diagnosed and where to get the treatment… I think
earlier access to testing, respondents indicated clearer information that the major thing … that [TB] is existing, and [services] are free….…”
about TB and where to access reliable testing services at no cost to pa (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 people Several family and community influences were reported to prevent
with DR-TB, which worsens their cases. They will be treating malaria, access to testing. Respondents cited instances in which patients’ parents
typhoid [fever]… making some mistakes costing people their lives. But, or spouses acted as a barrier to appropriate care, sometimes because of
assuming the knowledge of TB is everywhere… it will be easy for [private their own beliefs in alternate care, a lack of awareness about the TB
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 …[and] procedures, and misdiagnosis due to low index of suspicion in both
that everything is free. I didn’t believe that …my mummy asked if I would public and private hospitals. The attitude of public healthcare workers
come I said no, I was not coming but [eventually I came and].. [my was also a cited as a barrier.
health] has improved … The patients coming here are happy … that is why
“The first day I went for [a] test….…they chased me out that I should go
we are suggesting radio advertisement or TV …” (Patient FGD).
and stay by the window…I felt embarrassed ...why should I be disgraced
“My advice is that there should be awareness through the radio or tele
to stay outside ...they ordered me to buy [a] handkerchief to cover my
vision that whoever that coughs should visit hospital that it is free because
mouth … they chased me away” (Patients FGD).
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 There were particular instances of adult females living with their
Participants mentioned several patient-level reasons for difficulty parents, who were prevented from accessing treatment. In one instance,
getting diagnosed after testing. A predominant theme was preference for the duration of treatment was a barrier, and the parent thought going to
private sector care or long wait times for test results in the public sector, a prayer house would bring faster results. In the other instance, the fa
which led to the seeking of alternate care elsewhere. A second important ther believed his daughter was already healed by prayer and not in need
theme was not being able to pay transportation costs to return for of any medication.
appointments. Family responsibilities and fear of separation, school and work
conflicts were also mentioned as barriers to starting treatment.
“I got there for sputum culture, at government hospital they said [for] this
At the health system level, limited hospital bed spaces to admit pa
[test], you will have to come back for it. They will have to be giving us [a]
tients in the initial phase of treatment contributed to delays in treat
date to come back for the sputum, they will say come back another day, if
ment. HCWs also mentioned staff workload and low motivation, due to
you get there again they will say you came late, and this thing is disturbing
unpaid salaries, resulting in slow case management.
me up to the extent that I could not walk, people will have to hold me, until
they said go somewhere else” (Patients’ FGD). “From the provider’s side is a lack of motivation. Imagine you are going to
attend to a patient every day for … 20 months, that means you abandon
At the interpersonal level, there were instances of families removing
almost all you have to do for that patient. And in a situation where sal
patients from the care cascade to seek alternatives in traditional healing
aries are not forthcoming and the support from the [funding] partners are
and prayers, or the patients themselves preferring alternative care to the
[much]. The program pays the DOTS providers [5USD] communication
DR-TB care offered publicly. These are discussed in cross-cutting themes
allowance monthly but there is a very good package for the patients [105
below. While these family influences were sometimes negative, there
USD]. … Most of the providers in the face of no salaries will … envy what
were also responses indicating that parents had to be persistent to get
the patients are getting… So, from the provider side this is one of the major
their children diagnosed.
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
3.2.5. Gap 4: from treatment initiation to treatment completion
[other daughter] started coughing, they were taking her to several hos
At the individual level, several respondents mentioned that adverse
pitals, until they got to general hospital …. [For] months, they asked [the
drug reactions were a major issue with adhering to the treatment
mother] to come back, … she was always going and coming, asking
regimen. These led to some instances of patients losing hope or
[about] the result [and] they always said nothing. [Much] later, [they]
becoming anxious and refusing further treatment or dying while on
called the mother [with the result]” (Patients FGD).
treatment.
At the health system level, the predominant themes were prolonged
“[An elderly man], … when he sees the tray for drugs, … he will start
laboratory delays and errors, as well as negative healthcare worker
vomiting, ha! even when they have not given him, as soon as he sees it, he
attitudes.
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 … information. color of the doctors or nurses uniform he will be so afraid…he said it is
They [will] say …drop your sample in the lab .. and go and … come back better for him to go [home] and die… maybe he is dead but we don’t
tomorrow or come back on Friday, [and] today is [only] Monday…[they know… they gave him [the] paper to sign out of treatment…and he signed
will say] come back next week (HCW KII). out and left” (Patients FGD).
“Some [government] hospitals …were always postponing appointments,
An initial 8 months hospitalization was the standard practice before
treating people like animals…they shout on us not to stand somewhere,
2013 and is still used for certain high risk patients e.g. pediatric cases
touch anything, or …go out, come back tomorrow, up to the extent that I
and those who are pregnant or have co-morbidities. Transitioning be
had given up … but … a month after I got the test after disturbing them,
tween the initial hospital phase and continuation in outpatient care was
but some people do not have the perseverance to do what I did….…please
also another point at which patients dropped off treatment, sometimes
help us to explain to [HCWs] to treat [patients] well” (Patients FGD).
due to miscommunication or poor understanding of the process.
“…a lack of information caused my stopping the treatment, due to…

3.2.4. Gap 3: from diagnosis to treatment
lapses on their sides… because … after they discharged me I was [told] to
Barriers to treatment initiation occurred at individual, family and
go [to] the community- who are the community I don’t know,… [that] is
health system levels, many of which were also cross-cutting, such as
their medical term…[I] am not a medical person. How do I get to know all
preference for private sector care. At the individual level, some partic
those things? …that was how I actually stopped… taking my medication”
ipants recalled knowing patients who died before they could initiate
(Patients FGD).
treatment due to delayed diagnosis. A few instances were cited of pa
tients refusing treatment or giving false addresses because of fear of long Weak linkages and referral systems led to patients dropping off
treatment duration or belief in alternative care, particularly traditional treatment when moving between facility and home. One instance
or spiritual healing. involved a prisoner released from jail who was subsequently lost to
follow-up.
“Sometimes … there are some people … they [say they] know what their
problem is. [They] came to [the hospital but] gave [a] fake address and
3.2.6. Cross-cutting barriers across the care cascade
phone number … I think this quarter alone … I have lost 3 [patients] like
Several cross-cutting barriers were identified. At the individual level,
that. The last conversation we had was that they know their problem was
these included attributing symptoms to other causes or perceptions
[a spiritual attack] from their village and [they] are going to [the 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 collect
related to the influence of parents, spiritual leaders and to a lesser de injections at the right time; if anything happens to us or we feel anything,
gree, husbands. Although predominantly negative, these experiences we go to meet them. They [joke] with us, allowing us to realise that we are
were sometimes positive. still humans and that there is still hope for us here…” (Patients FGD).
“They attend to us as if we are their [relatives]. There is no stigmatisa
“My pastor, he told me to come to the [treatment center], that this cough I
tion… I don’t know of other centres but they don’t separate themselves
am coughing that he has seen someone that was coughing the same and
[from us here]. If at times we [don’t] use our mask, they talk to us …,
had been collecting drugs for six month and it stopped.It was my pastor
attend to us. They don’t … shout at us [or] make us feel different”
that knew about it and ask me to come.” (Patients FGD).
(Patients FGD).
“We have had a case of a pastor who refused … a member of his church
from taking drugs for DR-TB when the patient actually has DR-TB. He The provision of free DR-TB care and patient financial support was
refused vehemently that it was not a disease to be cured like that, that it mentioned repeatedly by patients and their relatives as the main facil
was a special [problem]. But … eventually [the pastor] himself came itator to care.
down with DR-TB and died” (HCW KII).
“…when I remember [what I went] through [with] my daughter, how they
Parental influence was a particular problem across the care cascade, [referred] us from [one hospital] to [another]. [An] ordinary razor
affecting even adult patients, especially if they were female. This was blade, before they will give you … you go and pay in to the [hospital]
often due to the parents own perception of better results with alternative account … but, I thank God for [the program]. They make me to be the
care. happiest woman on this earth because [to] lose a child of … 15 years
[would] not [have been] easy but today they put laughter into my own
“I had an experience….… a patient ... was ... asked ..to go and do... a
family… Thank you.” (Treatment supporters FGD).
[further testing] ….the mother insisted that it is ...a spiritual attack...and
“The day they gave me the result and said it was TB, I was like ah, and I
all effort to ensure that.. the patient takes treatment, failed” (HCW KII).
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
what gave me the opportunity to come here” (Patient FGD).
“The man who spoke with you earlier is [the patient]’s father. God has
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 of 3.2.7. Program strengths
peace.” (Relative to patient not initiated on treatment). Overwhelmingly, patients cited the free care and financial support
provided by the program as the major facilitators of access, enabling
Healthcare workers and program managers also mentioned the lack them to focus on getting better, without the added worries of compen
of female autonomy to seek care without their husbands’ approval. 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 [a] On the other hand, healthcare workers mentioned teamwork and
waste [of] time, until the sickness [has made her bedridden].” (HCW coordination, pooling of resources from implementing partners, the use
KII). of technology e.g. WhatsApp messaging within the team to improve
patient tracking and GeneXpert results notifications.
When female patients were asked directly, none of them mentioned
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, it
tudes, knowledge and skills of providers, which affected linkage and 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
contributes to the understanding of the main factors influencing access
Attitudes of healthcare workers, from the perspectives of patients, and retention in care for DR-TB patients and brings to bear the impor
were predominantly negative before diagnosis. tance of targeting control efforts at different stages of the care cascade.
Although numbers improved over the period of study, only 2.5% of
“When this [illness] started… when I went for [a] test … I was treated
people with DR-TB successfully navigate the DR-TB care cascade in
anyhow, like sit here, leave here, shouting, and I fought them to stop
Nigeria. The vast majority do not even make it to formal providers. Our
chasing me … and embarrassing me” (Patients FGD).
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 the
them into care, similar to studies from South Africa and India [37,38]. 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 first
sector, including with spiritual and traditional healers, have been shown step for TB control in Nigeria, since case-finding is reliant on patients
to dramatically improve TB case finding (up to 100%) in resource- recognizing their symptoms and presenting to a public health facility
limited settings like Nigeria [39–41]. with TB services. This is supported by other studies from Nigeria, calling
Our data suggest an estimated thre quarters of DR-TB patients are for improved public communication around TB [65–67]. Mass aware
lost at Gap 2 due to misdiagnosis or inadequate provider index of sus ness campaigns have been used sucesfully in South Africa and other
picion, poor provider attitudes, clinic and laboratory challenges and the settings to create awareness, reduce stigma, and improve case finding
poor linkages between the private and public sector. Patients also [56,68,69]. Improving accessibility to healthcare facilities with TB
mentioned fear of prolonged treatment. Provider training and supervi testing and treatment could include active case-finding, mobile TB
sion contributed to significant increases in case finding in India and clinics and working with the private sectors to ensure adequate support
Ethiopia [40,42]. for referring TB patients for appropriate testing. Interventions might
According to the care cascade, the majority of people diagnosed with also include behavioural change messages, advocacy with community
DR-TB (64%) went on to initiate treatment and 78% of these finished leaders and gatekeepers [70]. Improving access to TB care services for
treatment. Gaps 3 and 4, treatment enrolment and completion, were women and children need to consider adverse cultural gender and
sometimes due to individual beliefs and perceptions about healthcare, parental norms, especially those that could prevent them from accessing
and fear of treatment, as well as work and family commitments. This healthcare. Integrating current policies to protect the rights of women
highlights the need to continuously counsel patients, especially on and children to access TB care could potentially improve their health
adherence and potential side effects, and to address the opportunity protection [71,72].
costs of accessing care, as this has been shown to improve retention in
care [43]. The financial support given to patients was repeatedly cited as 4.1. Comparing different sources of data
a major facilitator at this stage and needs to be sustained.
Related to treatment completion, patients’ mental health and the toll Findings from the quantitative data were generally in agreement
from medication side effects were underscored by several respondents. with qualitative findings. Overall, the quantitative findings indicating
The toxicities of DR-TB medications and their effects on patients’ out that males and adults were more likely to progress through the various
comes is widely documented [25,44,45]. The current revision in WHO steps of the cascade were reflected in the qualitative themes showing
guidelines to shorter oral regimens will potentially improve patient 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 dren were more likely than adults to initiate treatment once diagnosed
gender roles impeding access to TB care for women [53,54]. in the South-West zone, but not at the national-level. One likely reason
While each level had unique barriers, addressing the cross-cutting might be the particular attention given to initiate pediatric patients on
barriers could serve as a first step for policy change and targeted in treatment once tested within the South-West zone. This earlier treat
terventions. For example, at each level of the cascade, patient beliefs and ment initiation in children might not be a complete contradiction as the
perceptions about the symptoms and the path to cure determined cascade analysis showed a reduced likelihood of progressing from tested
whether they persisted to treatment completion or not. Patients and to treatment outcome, and not just treatment initiation alone.
providers repeatedly recommended improving community awareness
on TB. This would likely have impact across the continuum of care, as
10
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. Funding
Our study has some limitations. The quantitative data for incidence
and access to testing are estimates using routine data. This may have COO received funding for field work through the Global Fund New
introduced bias into cascade gaps because as estimates, they do not
Funding Model MDRTB Grant (Global Fund to Fight AIDS, Tuberculosis
account for the changing patient populations at each stage of the cascade and Malaria: NFM MDRTB Grant), with funds provided through IHVN as
[8]. The cohort analysis used in the second step links diagnostic to
the Principal Recipient. The funders had no role in study design, data
treatment registers and tracks patients to treatment completion. This collection and analysis, decision to publish, or preparationof the
may have minimized bias in the cascade estimates at the later stages of
manuscript.
the cascade.
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 CRediT authorship contribution statement
fact that we conducted interviews in only 2 out of 6 geopolitical zones
in Nigeria, the extent to which our results are generalizable to other Charity Oga-Omenka: Conceptualization, Methodology, Formal
parts of the country is largely unknown. Additionally, given their status analysis, Visualization, Writing - original draft. Jody Boffa: Methodol
as ‘missing’, we were unable to seek direct feedback from people who ogy, Writing - original draft. Joseph Kuye: Software, Validation,
did not present to health centres. Although the perceptions of those Writing - review & editing. Patrick Dakum: Resources, Writing - review
receiving care provide insight into the reasons for these gaps, we may & editing. Dick Menzies: Methodology, Supervision, Writing - original
have missed potetntial factors that affect the large proportion of losses draft. Christina Zarowsky: Conceptualization, Methodology, Supervi
at the first stage. sion, Writing - original draft.
Although participants were further probed and their responses
reconfirmed, we cannot exclude the possibility of recall and reporting
Acknowledgements
biases. We addressed this by triangulating sources, location and
interview methods. There was an overall consistency in the themes
The authors thank the National TB and Leprosy Control Program
emerging from the different sources of data. Finally, we did not
(NTBLCP) of the Federal Ministry of Health (in Abuja, Plateau and
conduct interviews in Northern Nigeria beyond the central geopolitical
OgunState), the International Research Center for Excellence (IRCE) of
zone. There is a possibility that particular contexts in these regions
the Institute of Human Virology Nigeria(IHVN) for granting access to the
were not explored.
National database and for support in the process of data collection.
The contents of this publication are solely the responsibility of the
5. Conclusion
authors and do not necessarily represent the official views of the Global
Fund, NTBLCP or IHVN.
Our study has shown that, although there is noticeable progress in
access to DR-TB care in Nigeria between 2013 and 2017, this is not
Appendix
nearly enough to meet the End TB targets. On average, less than 3% of
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
11
Table A1
C. Oga-Omenka et al.
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 health
Reaching 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
12
Qualitative interviews with

providers of DR-TB care at the
health center and community
levels

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)
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14
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
Contents lists available at ScienceDirect
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Mycobacterial Diseases
journal homepage: www.elsevier.com/locate/jctube
Erratum regarding previously published articles
The Declaration of Competing Interest statements were not included Academy Experience (Volume 20C, August 2020).
in the published version of articles that appeared in the 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 21C, Quantitative structure-activity relationship (QSAR) and molecular
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.

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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 ScienceDirect

Journal of Clinical Tuberculosis and Other

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

Available online 9 October 2020

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.

“…a lack of information caused my stopping the treatment, due to…

“What we heard about TB before the arrival of [the] TB center is that

Qualitative interviews with

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

In-depth interviews with patients

providers of DR-TB diagnosis and

treatment at the health center

Gap 5: Number of individuals who experienced post-

and community levels

[5] Onyedum CC, Alobu I, Ukwaja KN. Prevalence of drug-resistant tuberculosis in

treatment TB recurrence or death

up in the intensive and

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

Ministry of Health Health. DoP; 2015 August 2014.

[20] WHO. Global tuberculosis report 2016. 2016.

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

treatment initiation among drug-resistant tuberculosis patients in Nigeria-a

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-

[35] NBLCP/FMOH. e-TB Manager Treatment Database. Nigeria: National Tuberculosis

Contents lists available at ScienceDirect

Journal of Clinical Tuberculosis and Other

Erratum regarding previously published articles

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.

Available online 6 May 2021

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