Pulmonol.

2018;24(5):294---299

www.journalpulmonology.org

ORIGINAL ARTICLE

Diagnosis delay of tuberculosis in the Huambo

province, Angola
E. Santos a,b,∗ , Ó. Felgueiras c,d , O. Oliveira b , R. Duarte b,e,f

a
Instituto Superior Politécnico, Universidade José Eduardo dos Santos, Cidade Alta, Huambo, Angola
b
EpiUnit --- Instituto de Saúde Pública, Universidade do Porto, Rua das Taipas, n◦ 135, 4050-600 Porto, Portugal
c
Departamento de Matemática, Faculdade de Ciências, Universidade do Porto, Porto, Portugal
d
Centro de Matemática da Universidade do Porto, Porto, Portugal
e
Departamento de Pneumologia, Centro Hospitalar de Vila Nova de Gaia/Espinho, EPE, Vila Nova de Gaia, Portugal
f
Departamento de Ciências da Saúde Pública e Forenses e Educação Médica, Universidade do Porto, Porto, Portugal

Received 8 March 2017; accepted 8 October 2017

Available online 3 January 2018

KEYWORDS Abstract
Tuberculosis; Introduction: Early diagnosis is necessary for the success of the tuberculosis (TB) program.
Diagnosis; Goal: To identify factors associated with diagnosis delay of TB in Huambo, Angola.
Associated factors; Material and methods: Cross-sectional study carried out in patients diagnosed with TB at the
Huambo Huambo Anti-Tuberculosis Dispensary (ATD) in the period between October 2015 and January
2016.
Results: The 247 patients included in the analysis had a median age of 27 years and a median
diagnosis delay of 64 days. In the univariate analysis, age, consumption of alcoholic beverages,
living in a residence further than 10 km from a healthcare unit, and looking for any other health
unit than the emergency unit were associated with longer diagnosis delay. In the multivariate
analysis model, to be between 30 and 44 years of age (p = 0.018), to live in a residence more
than 10 km from a healthcare unit (p = 0.006) and to turn to traditional medicine as the first
healthcare option (p < 0.001) were factors that led to greater time delay before diagnosis.
Conclusions: In the Huambo province, age, distance to healthcare facility and the first health-
care service consulted were associated with diagnosis delay of TB.
© 2017 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L.U. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).

∗
Corresponding author.
E-mail address: [email protected] (E. Santos).
https://doi.org/10.1016/j.rppnen.2017.10.002
2531-0437/© 2017 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L.U. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Diagnosis delay of tuberculosis in Huambo, Angola 295

Introduction The Huambo province has a regional mycobacteriology

laboratory that performs culture tests and antibiotic sen-
Tuberculosis (TB) is a public health problem that affects sitivity tests (TSA) in the case of a negative microscopy,
millions of people worldwide1 especially in sub-Saharan therapeutic failures or resistance to antibiotics in the Cen-
Africa where the burden of TB is greater.2 For an effective tral South region.
TB control program it is essential to obtain early diagno- The purpose of this study was to identify the factors asso-
sis, immediately begin appropriate treatment and ensure ciated with TB diagnosis delay in the population of Huambo,
its continuity.3 Angola.
Time delay in the diagnosis of TB plays an important role
in the increase of infectivity, mortality risk and transmission Methodology
of the disease in the community.4,5 It is estimated that an
untreated patient with positive microscopy for TB bacillus Study design
can infect, on average, 10---15 community contacts within a
year.6
Cross-sectional study including patients diagnosed with TB in
The factors that contribute to the time delay in the
the Huambo ATD, between October 2015 and January 2016.
diagnosis and treatment of TB may be related to the
patient himself as well as the healthcare service.7---12 Sex,
Inclusion and exclusion criteria
age, educational level, occupation, distance from home to
All patients diagnosed with TB of all forms, who appeared
the healthcare institution, co-morbidities and poor knowl-
in the Huambo ATD, at the time of application of the ques-
edge about TB, were some of the factors related to the
tionnaires, participated in the survey regardless the time
patient.13---16 Lack of diagnosis resources, such as chest radi-
of treatment. Included in this study (new and previous
ology, negative microscopy result, waiting time and the first
treatment) are all ages and both gender. Patients with-
healthcare unit consulted were associated to the system
out complete information for the time delay variable were
delay.8,10,15---17
excluded from the analysis.
In Angola, TB is one of the main reasons for visits to
healthcare services. In 2015, the incidence of TB was 93
per 100,000 inhabitants.18 In 1981, the Angolan Ministry Place of study
of Health established the National Tuberculosis Program The study was conducted at the ATD, and at the Sanatorium
(NTP), whose priority was the establishment of TB diagno- Hospital of Huambo.
sis and treatment services throughout the country.8 Huambo
province is located on the central plateau of Angola, with Data collection
an area of 35,771 km2 and 2,019,555 inhabitants, corre- Data was collected through the distribution of question-
sponding to 7.8% of the total population of the country, naires. Patient files and TB treatment cards were also
according to the final results of the population census of reviewed. A questionnaire was developed for data collection
2014.19 The province’s healthcare network consists of 11 and filled out by the patients at the time of their monthly
municipal hospitals, 1 General/Provincial hospital, 1 Sana- follow-up appointments and by hospitalized patients if they
torium hospital, 1 Anti-Tuberculosis Dispensary (ATD), 50 were diagnosed in the study period. This task was per-
healthcare centers and 165 health posts (report from the formed over the course of 22 days by the technicians working
provincial directorate of health, 2016). For the diagnosis in the TB area, who received a specific training seminar
and treatment of TB, the province has 12 outpatient units, by the researcher. Patients were individually questioned
some of which are linked to municipal hospitals. In these in a closed environment on the unit’s premises, to main-
units, pulmonary TB diagnosis is based on sputum microscopy tain patient privacy, after the clarification on the study
performed on three patient-provided samples, clinical his- and informed consent. The questionnaire included socio-
tory and chest radiography. For extrapulmonary TB (EPTB), demographic information, risk factors for the disease and
the diagnosis is based on microscopy of biological products clinical characteristics. The clinical information was col-
depending on the infected organ or only on the symptoms of lected in the patients’ files as well as some additional
the disease, the clinical history and the radiography, at the sociodemographic information contained therein, obtained
doctor’s discretion. Patients with criteria for hospitalization before and after to survey.
due to complications of TB or requiring further intervention
are referred to the sanatorium hospital, since it is the ref- Sample
erence unit. Patients without criteria for hospitalization are 464 patients were diagnosed during the study period and
directed to the ATD. Treatment is provided under directly 353 responded to the survey. Of the subjects surveyed, 247
observed treatment (DOT) during the intensive phase. In patients were selected for this study.
the maintenance phase, the patient is entrusted to a
relative.
Definition of variables
The Sanatorium hospital, with its ambulatory depend-
ency ATD, is considered the reference center for TB in
The diagnosis of TB refers to the recognition by health work-
the region. The Sanatorium Hospital/ATD possesses a bac-
ers of an active case, to a patient with current disease due
teriology laboratory for microscopy exams and a radiology
to M. tuberculosis.20
section.
296 E. Santos et al.

Diagnosis delay was defined as the time between the the diagnosis could not be calculated. The median age
onset of signs and symptoms of TB and the diagnosis (patient of these patients was 25 years and 75 (71%) were male.
delay + healthcare delay). Excluded patients differed from the included ones especially
In the municipality variable patients were split into in tobacco use (lower proportion of non-smokers, p = 0.005),
those who lived in Huambo city and those who lived out- qualifications (higher proportion of illiterate and primary
side, including the other ten municipalities of the Huambo educated, p < 0.001) and the first healthcare unit sought
province and those from other provinces in Angola. (higher proportion of Health Center and Emergency Service,
Age was categorized into four classes: <15 years, 15---29 p < 0.001).
years, 30---44 years and >45 years. Occupation was defined
as regular occupation and included individuals with fixed
employment, retired (since they have regular pensions) Discussion
and students. Individuals without fixed employment or with
irregular services such as street vendors, peasants and oth- In this study the time delay of 247 diagnosed patients at the
ers were considered as having non-regular occupation. Huambo ATD, between October 2015 and January 2016 was
The clinical presentation of TB was defined as pulmonary evaluated.
and extrapulmonary TB. The median diagnosis delay was 64 days. Our findings do
not differ from other studies in Nepal,21 Ethiopia,10 India,12
Statistical analysis Yemen,22 and Zambia23 where the median delay was 60---63
Univariate and multivariate linear regressions were per- days. On the other hand, Tanzania24 had a considerably
formed with the response being the logarithmic transfor- longer median time of 136 days and Portugal25 a shorter one
mation of the time delay. For the multivariate analysis of 36 days. A previous study conducted in Luanda, Angola,
the complete model was determined based on a selection had a median diagnosis delay of 45 days.8 The factors
of variables, using the stepwise regression method that associated with delaying the diagnosis of TB may be differ-
minimizes the AIC (Akaike Information Criterion). All data ent between Huambo and Luanda, considering the greater
analysis was performed with R version 3.3.2 software and concentration of the population in the country’s capital (72%
p-value <0.05 was considered significant. living in urban area).
In the univariate analysis, we found that living outside of
Huambo city, being between 15 and 29 or 30---44, consuming
Ethics approval
alcoholic beverages, living in a residence more than 10 km
from a healthcare unit and seeking health care outside of
The study was approved by the General Directorate of the
the emergency service system were associated with longer
Sanatorium Hospital of Huambo, Angola and the Ethics Com-
diagnosis delay.
mittee of the São João Hospital Center and the Faculty of
Based on the multivariate analysis results encountered,
Medicine of the University of Porto, Portugal.
belonging to the 30---44 years old age group was associ-
ated with a longer time delay until diagnosis. Age has been
Results associated with diagnosis delay in other studies.9,10,14---16,24,25
Several social factors such as work schedule and difficulty
Of the 353 respondents, 247 patients were included in this in organizing working time to visit healthcare services have
study. Their median age was 27 years old, 159 (64%) were been given as explanations for a greater delay in this age
males, 197 (80%) had irregular occupations, 136 (55%) had group.15
a household size of 5---8 people, 151 (57%) patients did not Regarding the distance to the healthcare service, in the
consume alcoholic beverages and 204 (83%) did not smoke studies carried out in Ethiopia and Tanzania, the patients
(Table 1). who lived more than 10 km away from the healthcare insti-
The median diagnosis delay was 64 days (IQR: 37---95 tutions had a longer time delay until the diagnosis of TB,
days). when compared to those living within a 10 km radius.17,24
In the univariate analysis, living outside of Huambo Other studies have found a relationship between longer
(p = 0.006), being aged between 15 and 29 (p = 0.035) or walking distance to a healthcare facility and patient delay in
30---44 (p = 0.005), consuming alcoholic beverages (p = 0.039) Nepal,14 Nigeria,16 Odisha, India11 and south India.12 These
and living in a residence more than 10 km from a healthcare studies corroborate our findings, in which the distance from
unit (p = 0.001) were associated with longer diagnosis delay. the healthcare service was considered a factor in diagnosis
Using the emergency unit as a reference, it was found that delay due to unavailability and lack of access to TB diagnosis
the patients who first sought out any other healthcare unit and treatment units in rural areas.
took more time until diagnosis (p ≤ 0.014) (Table 1). The first healthcare service consulted was identified as
The multivariate analysis model indicated that indi- the risk factor for longest delay until diagnosis, particularly
viduals aged between 30 and 44 years (p = 0.018), living if it was a private clinic or a traditional healer. Though most
at a distance greater than 10 km from a healthcare unit patients (78.9%) lived in the Huambo municipality, we can-
(p = 0.006), and not going to the emergency unit, especially not say whether the demand for these units is attributable
if they first used traditional medicine (p < 0.001), had longer to patients living in rural or urban areas. Although the num-
diagnosis delay (Table 2). ber of patients that consulted the health center (17%) and
One hundred and six patients were excluded from the traditional healer (5%) is low, there is a longer delay time.
analysis because they did not know the date of the onset Similar results were also verified in the previous study in
of their symptoms, which meant that the time delay until Luanda. This was also confirmed in previous studies, where
Diagnosis delay of tuberculosis in Huambo, Angola 297

Table 1 Sociodemographic and clinical characteristics associated with the time delay until TB diagnosis in the Huambo Province,
Angola.
Patient characteristics n (%) Time mean (s.d.) Univariate analysis

Exp (coef.) (p-value) 95% IC

Municipality
Huambo 195 (79) 74.4 (49.9)
Outside of Huambo 52 (21) 101.2 (79.1) 1.30 (0.006)* (1.08, 1.57)
Sex
Male 159 (64) 83.0 (58.5)
Female 88 (36) 74.7 (57.6) 0.88 (0.136) (0.75, 1.04)
Qualifications
Illiterate 24 (10) 84.5 (65.7)
Primary school 60 (24) 83.2 (53.6) 1.05 (0.744) (0.78, 1.41)
High school (1C) 74 (30) 78.9 (62.5) 0.94 (0.673) (0.71, 1.25)
High school (2C) or + 89 (36) 78.5 (56.1) 0.97 (0.837) (0.73, 1.29)
Age
<15 years 16 (6) 56.3 (51.0)
15---29 years 121 (49) 78.6 (57.1) 1.41 (0.035)* (1.03, 1.94)
30---44 years 79 (32) 89.3 (60.9) 1.60 (0.005)* (1.15, 2.23)
45 or + years 31 (13) 74.6 (56.7) 1.33 (0.129) (0.92, 1.93)
Occupation
Irregular occupation 197 (80) 81.1 (57.3)
Regular occupation 50 (20) 76.2 (61.9) 0.91 (0.341) (0.75, 1.10)
Number of household members
Till 4 people 69 (28) 85.7 (60.5)
Between 5 and 8 people 136 (55) 79.5 (59.5) 0.91 (0.313) (0.76, 1.09)
More than 8 people 42 (17) 72.8 (49.7) 0.85 (0.192) (0.67, 1.08)
Alcohol use
No 142 (57) 73.9 (53.5)
Yes 46 (19) 90.7 (63.6) 1.24 (0.039)* (1.01, 1.52)
Used to drink 59 (24) 86.7 (63.4) 1.14 (0.168) (0.95, 1.37)
Tobacco use
No 204 (83) 78.4 (57.6)
Yes 24 (10) 83.0 (63.2) 1.05 (0.709) (0.81, 1.37)
Used to smoke 19 (8) 93.7 (59.3) 1.23 (0.160) (0.92, 1.65)
Distance
Under 1 km 32 (13) 54.9 (26.6)
Between 1 and 10 km 131 (53) 73 (50.1) 1.22 (0.095) (0.97, 1.53)
Over 10 km 84 (34) 100.7 (71.3) 1.65 (0.000)* (1.29, 2.10)
First searched unit
Emergency Service 13 (5) 39.2 (12.8)
Outpatient Hospital Service 131 (53) 64.8 (43.6) 1.47 (0.014)* (1.08, 2.01)
Health Center 48 (19) 78.3 (49.6) 1.79 (0.001)* (1.28, 2.49)
Private Clinic 42 (17) 117.2 (65.9) 2.70 (0.000)* (1.93, 3.79)
Traditional Medicine 13 (5) 161.4 (88.1) 3.67 (0.000)* (2.42, 5.56)
Detection
Passive tracking 217 (88) 82.2 (59.9)
Active tracking 30 (12) 65.0 (41.4) 0.84 (0.138) (0.66, 1.06)
Clinical presentation
Pulmonary 234 (95) 80.0 (58.4)
Extrapulmonary 13 (5) 81.2 (55.6) 1.04 (0.826) (0.73, 1.47)
298 E. Santos et al.

Table 1 (Continued)

Patient characteristics n (%) Time mean (s.d.) Univariate analysis

Exp (coef.) (p-value) 95% IC

Microscopy
Positive 186 (75) 80.4 (57.9)
Negative 35 (14) 82.4 (57.9) 1.03 (0.789) (0.82, 1.29)
Without microscopy 26 (11) 74.4 (62.1) 0.88 (0.320) (0.68, 1.13)
Serology HIV
Positive 21 (9) 81.4 (50.7)
Negative 197 (80) 81.3 (61.8) 0.95 (0.736) (0.72, 1.26)
Unknown 29 (12) 70.8 (33.0) 0.94 (0.709) (0.66, 1.33)
Family support
No 72 (29) 85.8 (58.8)
Yes 175 (71) 77.7 (57.9) 0.89 (0.186) (0.75, 1.06)
* p-Value <0.05.

Table 2 Factors associated with the time delay until TB diagnosis in the Huambo Province, Angola.
Factors Multivariate analysis Exp (coef.) (p-value) 95% CI
Age
<15years 1
15---29 years 1.27 (0.090) (0.96, 1.68)
30---44 years 1.41 (0.018)* (1.06, 1.88)
45 or + years 1.30 (0.107) (0.94, 1.80)
Distance
Under 10 km 1
Between 1 and 10 km 1.14 (0.229) (0.92, 1.40)
Over 10 km 1.36 (0.006)* (1.09, 1.70)
First searched unit
Emergency Service 1
Outpatient Hospital Service 1.38 (0.038)* (1.02, 1.88)
Health Center 1.60 (0.006)* (1.15, 2.23)
Private Clinic 2.36 (0.000)* (1.68, 3.31)
Traditional Medicine 3.22 (0.000)* (2.12, 4.88)
* p-Value <0.05.

longer diagnosis delays were obtained when private health- time was calculated based on the dates declared by the
care facilities and traditional healers,11,12,17,24,26 were the patients, which may have been subject to error.
first healthcare unit used. On the other hand, in the Huambo Despite the limitations presented, the strengths of this
province, poor availability and accessibility of the primary study are relevant. The study was carried out in the refer-
health care, lack of public transport for some communi- ence unit that covers the region, with good adherence and
ties and socioeconomic conditions of the patients can be it is the first study on TB diagnosis delay in the Huambo
considered in the diagnosis delay. province.
Our study had some limitations. It was performed in an
area with insufficient resources. Patients who appeared at
the weekend were not questioned. Other limitations of our Conclusion
study were mainly related to the exclusion of the population
that did not remember the date of the onset of their symp- In the Huambo province, age, distance to healthcare units
toms. However, despite the fact that the excluded patients and the first healthcare service used were associated with
differ in their smoking habits, literary qualifications and first tuberculosis diagnosis delay. To reduce delays and improve
healthcare unit used, there were no differences between access to health care, efforts should be made to expand
the two groups in any of the other analyzed variables that public health institutions in rural communities, to decentral-
were significant in the diagnosis delay. We cannot exclude ize health services. The government, via Ministry of Health,
memory bias in the responses. We assume that the delay should create policies involving the private sector in TB care.
Diagnosis delay of tuberculosis in Huambo, Angola 299

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