Interdisciplinary Perspectives on Infectious Diseases
Volume 2019 (2019), Article ID 2154240, 14 pages
https://doi.org/10.1155/2019/2154240

Research Article

Total Delay in Treatment of Tuberculosis and Associated Factors among New Pulmonary TB Patients in Selected Health Facilities of Gedeo Zone, Southern Ethiopia, 2017/18

Netsanet Awoke, Bedado Dulo, and Feven Wudneh

Department of Medical Laboratory Science, Dilla University, P.O. Box 419/13, Ethiopia

Correspondence should be addressed to Netsanet Awoke; netawoke4@gmail.com

Received 26 January 2019; Revised 19 April 2019; Accepted 28 April 2019; Published 2 June 2019

Academic Editor: Massimiliano Lanzafame

Copyright © 2019 Netsanet Awoke et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Background. TB is an infectious disease caused by the bacillus Mycobacterium TB complex. It is a major public health concern causing devastating illness in millions of people each year and one of the top 10 causes of death worldwide following HIV pandemic. It demands huge costs each year for prevention, diagnosis, and treatment of TB. Global TB control progress depends on major advances in early diagnosis and treatment. Despite progress in providing diagnosis and preventive treatment of TB, big detection and treatment gaps remained with delayed diagnosis and treatment of TB especially in resource-limited countries. This is mainly because of factors related to the patient and health care system including sociodemographic, economic, and cultural barriers to accessing TB care. Objective. The study conducted in Gedeo Zone, Southern Ethiopia, had the primary purpose of identifying the median delay in starting a correct TB treatment and the associated factors for such a delay in patients newly diagnosed with PTB in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18. Methods. Institutional based cross-sectional study was conducted among new pulmonary TB patients in selected health institution of Gedeo Zone, Southern Ethiopia, 2017, from October, 2017, to May, 2018. All new pulmonary TB patients who fulfill the inclusion criteria during the study period were included in the study after informed consent was obtained from the participants. Data was cleaned, coded, and entered into SPSS version 20 for analysis. A frequency for variables was calculated. Chi-square was used to screen the possible potential associated factors and multivariate analysis was used to ascertain the association between variables. All statistical tests values of p<0.05 were considered as statistically significant. Result. The median total in treatment of TB was 60 days. Among the total study participants, 50.9% of the participants have unacceptable/longer total delay in TB treatment. Being of female gender, not attending formal education, having rural residency, having poor knowledge of TB, having home distance >10Km from the nearest health facility, visiting nonformal health care provider, and taking antibiotic treatment before TB diagnosis empirically were identified as significant independently associated factors for unacceptable total treatment in TB. Conclusions. There was higher median total delay in treatment of TB (60 days) and an overall prevalence of 50.9% unacceptable/longer total delay in treatment of TB. Female gender, rural residence, not attending formal education, visiting nonformal health facility as first health care seeking, having poor knowledge of TB, and having antibiotic treatment before TB diagnosis were identified as independent significant associated factors.

1. Introduction

Tuberculosis is an infectious disease caused by the bacillus Mycobacterium TB complex [1]. TB typically affects the lungs (pulmonary TB) but can also affect other sites (extra-pulmonary TB) including the meninges, kidneys, bones, and lymph nodes. It is most commonly transmitted via minute aerosol droplets of the bacilli that remain suspended in the air for prolonged periods of time, posing a particular infection-control challenge [1, 2].

The most commonly reported symptom of pulmonary TB is persistent (2 weeks or more) cough generally, but not always, with or without sputum production, chest pain, and sometimes blood (hemoptysis) [3]. In persons with TB, the cough is often accompanied by systemic symptoms such as fever, blood tagged sputum, night sweats, and weight loss [4]. Clinical manifestations of TB are dependent on a number of factors: age, immune status, coexisting diseases, immunization status to the bacillus, virulence of the infecting organism, and host-microbe interaction [1, 5].

Tuberculosis is a major public health concern worldwide, despite having a slow decline in incidence over the last decade [1]. Control of TB in the community depends on early diagnosis and treatment which is the key elements of the TB control program. Patients suspected with TB should be diagnosed and initiate treatment as early as possible. This is because of its importance for containing the spread of the disease within the community and for effective TB management [3].

The identification of TB cases depends on patients recognizing TB symptoms and seeking appropriate health care as well as the capacity of the health care system to early diagnose the disease. Missed opportunities for earlier detection and treatment of TB lead to increased disease severity for the patients [6] and a greater likelihood of transmission of M. tuberculosis plus multidrug resistance tuberculosis (MDR-TB) to family members and others in the community [4]. In addition, it may avert early mortality associated with more serious complications and severe disease due to delayed presentation [7]. This is because the majority of TB transmission occurs between the onset of cough and initiation of treatment, and patients become more contagious and result in ongoing transmission as the delay increases [2, 7].

Prevention of new infections of Mycobacterium tuberculosis and their progression to tuberculosis (TB) disease is critical to reduce the burden of disease and death caused by TB. Ensuring widespread patient access with fast turnaround time and high-quality diagnosis and early treatment is required for effective TB control [2]. In regions where high prevalence of TB, an early diagnosis is considered as one that is performed between 2-3 weeks after the onset of TB clinical symptoms and a late diagnosis is that performed 4 weeks after the onset of symptoms which is unacceptable diagnosis delay and is not recommended for effective TB control [8].

Currently, although sputum smear microscopy remains the most widely available test to establish a microbiological diagnosis, other more sensitive means of identifying M. tuberculosis, particularly culture and rapid molecular tests, are rapidly gaining acceptance as their performance and applicability are increasingly understood [1, 4]. To create access to the diagnostic and treatment services for MDR-TB, TB culture and drug-susceptibility test laboratories as well as MDR-TB treatment centers have expanded globally, including Ethiopia [2, 9].

In 2016, despite the increases in notifications of TB globally, big detection and treatment gaps remain. This may be due to underdiagnosis or delayed diagnosis and initiation of treatment because of barrier to accessing TB diagnostic and treatment service [6]. Delay in diagnosis and treatment of TB/total treatment delay is mediated by factors related to the patient and health care system [10]. Sociodemographic, economic, and cultural barriers to accessing TB care such as limited knowledge about signs and symptoms of TB, low health seeking behavior of the patients, complex diagnostic procedures, poor diagnosis with long patient waiting time, and difficulty of disease management in health facilities were reported as delay in treatment [2, 7, 10]. So, to fill this TB control gap, in 2015 WHO launched a new global TB strategy “End TB Strategy by 2035”. To achieve the milestones of End TB Strategy by 2035, one of the pillars is integrated early diagnosis and treatment of TB including systematic screening of contacts and high-risk groups and universal drug-susceptibility testing plus early initiation of treatment for all people with TB supported with intensified research [2].

Despite the findings of previous studies investigating the same topic, the study describes the situation of a specific setting, thus strongly related to its particular situation. The importance of the findings is mainly in the possibility of describing the situation of an area where TB is still a high prevalence disease, with a significant risk of underestimation or incorrect treatment. So, the study had primary purpose of identifying the median delay in starting a correct TB treatment and the associated factors for such a delay in patients newly diagnosed with PTB patients in selected health facilities of Gedeo Zone, Southern Ethiopia.

2. Materials and Methods

The study was conducted among new pulmonary TB patients in 8 selected health facilities (DURH, Yirgacheffe, Wonago, Gedeb, Bulie, Chelelektu, Chichu, and Harrorissa) of Gedeo Zone, Southern Ethiopia, from October, 2017, to May, 2018.

Institutional based cross-sectional study was conducted among 422 patients confirmed with tuberculosis infection in selected health facilities of Gedeo Zone who fulfill the inclusion criteria during the study period. Study participants of ≥15 years old & those new smear positive pulmonary TB patients who transferred into DOTS service of the selected health facilities were included. Study participants who were extra-pulmonary TB patients, ≤15 years old, who was critically ill and could not respond to the interview & who was transferred out to other health facilities for DOTS were excluded.

The health facility was selected based on the TB case report of the zone to fulfill the sample size with the specified data collection period. The total sample size was proportionally allocated based on its case report. The study participants, newly diagnosed as PTB patients, were consecutively recruited in each health center of TB clinic within the specified time period until the intended sample size was met. Number of patients to be interviewed from each health facility was based on the case load report or proportionately allocated to the selected health facilities based on their estimated annual flow of smear positive PTB patients.

3. Operational Definitions

Total delay in treatment: the time interval between the date onsets of major TB symptoms to first start of anti-TB treatment; in this case if the total delay in treatment is ≥ median total treatment, delay is considered longer/unacceptable delay.

New PTB: patients with two or more sputum smears/gene x-pert positive for acid fast bacilli and who had never received treatment for TB for as long as one month.

Nonformal health providers: these include traditional health providers (such as traditional injectors/healers, herbalists, spiritual/holy water).

Current smoker: an adult who has smoked 100 cigarettes in his or her lifetime and who currently smokes cigarettes. Beginning in 1991 this group was divided into “everyday” smokers or “somedays” smokers.

Former smoker: an adult who has smoked at least 100 cigarettes in his or her lifetime but who had quit smoking at the time of interview for the last 2 months.

Never smoker: an adult who has never smoked, or who has smoked less than 100 cigarettes in his or her lifetime.

Stigma: for each stigma question a score of 1= strongly disagree, 2= disagree, 3= agree, 4= strongly agree response was given. Those with a total score below the ≤25th percentile value of the total question’s were classified as having no/low stigma, those with score between 25th and 75th percentile value of the total question’s were considered as having moderate stigma, and those with ≥75th percentile value of the total question’s were considered as having sever stigma.

Alcoholic drinker: patients who drink presently or previously 5% alcohol with more than 500ml per days regularly.

Knowledge status: it is the knowledge of the patient regarding the means of transmission, symptoms, and prevention of TB. For each TB knowledge questions a score of one was given for yes response/for the correct answer and a score of zero was given for no response/for the incorrect answer. Then, total knowledge score and median were calculated. The scale was then dichotomized into two categories (good/below the median or poor knowledge equal or above the median) using the median as the cut-off.

Patient satisfaction: it is the previous satisfaction of study participants on health care provider and health care system. For each satisfaction question a score of 1= very low, 2= low, 3= medium, 4= good, or 5= very good response was given. Then a separate summary indicator was developed for analyses by dividing the total score into three strata, ≤25th percentile, between 25th and 75th percentile, and ≥75th percentile to label it as good, medium, and low, respectively.

Formal private health provider: private drug store, pharmacy, and private clinic opened with official licensed individuals.

Unacceptable/longer total treatment in TB: those who has total treatment delay greater than or equal to the median total treatment in TB (Asefa and Teshome, 2014; Yimer, Bjune and Holm-hansen, 2014; Mandi and Pradesh, 2012; Zeleke and Trifa, 2014).

4. Data Collection and Instruments

Study participants were informed clearly about the purpose of the study. A semistructured questionnaire (translated in English and to the local language) was prepared to interview patients; with this method, the investigators easily extracted data needed for the purpose of the study. Pretest was done on 5% of the sample size in none selected health facilities. The pretested questionnaire was used to collect information from study participants. Before the actual data collection process started, all data collectors (TB clinic nurse or health officer of respective health facilities and supervisors) was given two-day onsite training by the principal investigator on the purpose of the study and how to select study participants and fill the data collection tool. All eligible study participants were interviewed through face-to-face by trained data collector of the TB clinic in the selected health facilities just right after commencing treatment.

The questionnaire and the interviewers were supervised regularly throughout the duration of the study. The questions were open or close ended. For each patient, the following information was collected: sociodemographic characteristics, knowledge, and experience of stigma to TB.

Study participants also were asked to estimate the duration of experiencing pulmonary symptoms in days before first visit to the health facility (patient delay). In addition, they were asked the duration in days from first contact to healthcare providers until TB treatment initiation (health system delay). Finally, they were also asked to estimate the time in days they had been experiencing major pulmonary symptoms before presenting to health facilities with the current diagnosis of TB (total treatment delay). Moreover, they were asked about places they sought for treatment before first visit to the health facility, reasons for delay before visit to the health facility, and distance and time taken from their residence to the health facility.

Local religions and political and agricultural events were used as a calendar to collect information for those patients who were unable to estimate the date of onset of first presenting symptoms for the current diagnosis (TB).

5. Data Analysis and Interpretation

Data was checked for completeness and consistency in semistructured questionnaires. Then it was cleaned, coded, and entered using SPSS 20 for analysis. Frequency and cross-tabulation were checked to monitor data quality. Descriptive statistics was used to generate frequencies of categorical variables and summarize data. Tables were used for data presentation. Odds ratio with 95% CI was used to screen the possible associated factors.

Variation in categorizing of total treatment delay of TB has been documented. For the outcome variable, we used the median delay as a cut-off to dichotomize the TB patients into two groups (≥ median versus < median). The median of total delay was categorized as acceptable/shorter or unacceptable/longer total treatment delay. A patient for whom anti-TB treatment was not initiated within the median total treatment delay was considered to experience unacceptable total treatment delay [3, 11–16]. Identified variables were associated with experience of total treatment delay; P value ≤ 0.25 in bivariate analysis was candidate for final logistic analysis model. Multivariate analysis was used to ascertain the association factors. All statistical tests values of p<0.05 were considered as statistically significant.

6. Ethical Consideration

The study was approved by Dilla University, College of Health Sciences and Medicine, Research, Dissemination and Community Services Director Office (RDCDO). Ethical clearance was obtained from ethical review committee of Dilla University, College of Health Sciences and Medicine. Letter of support from RDCDO was delivered to selected health facilities administrators. Permission to undertake the research was obtained from the selected health facilities administrators. Moreover, the purpose of the study and benefits of the survey were explained for each study subject before data collection and written consent were obtained from each study participant. Confidentiality of information and privacy of the study participants were also maintained with interviewing each study participants in a separate place and coding to label individual respondents.

7. Quality Assurance

To ensure data quality, two-day training for data collectors was given before the start of data collection. The questionnaire was pretested in 5% of the sample size in none of selected health facilities in the zone. The investigators and supervisors followed data collection process regularly during the data collection to monitor overall activities of the data collection, to obtain the filled questionnaire and check for its completeness.

8. Results

8.1. Sociodemographic Characteristics of the Study Participants

Of the 422 eligible study participants, 235(55.7%) were males with a male to female ratio of 1.3 to 1. The mean age of study participants was 33 years, ranging from 15 to 70 years. Study participants with age group [14–24] years were 31.3%. Of the total study participants, 41.7%, 58.5%, 46.2%, and 40.8% of them were not attending formal education, having rural residency, being farmer, and having ≤500 mean monthly family income, respectively (Table 1).

Table 1: Sociodemographic characteristics of the study participants among selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Frequency (N= 422)
Percentage (%)

Sex of the participants

    Male
235
55.7

    Female
187
44.3

Age of the participants/ year

    15-25
132
31.3

    26-35
125
29.6

    36-45
104
24.6

    >45
61
14.5

Marital status of patients

    Married
234
55.5

    Single
170
40.3

    Others
18
4.3

Educational status/level

    Not attended formal education
176
41.7

    Primary school
144
34.1

    Secondary school
70
16.6

    Higher education
32
7.6

Religion of the study participants

    Orthodox Christian
94
22.3

    Protestant Christian
272
64.5

    Muslim
56
13.3

Study participants place of residence

    Urban
175
41.5

    Rural
247
58.5

Ethnicity of the study participants

     Gedeo
247
58.5

    Oromo
82
19.4

    Amhara
36
8.5

    Sedama
39
9.2

    Others
18
4.3

Occupation of the study participants

    Farmer
195
46.2

    Employed
56
13.3

     Daily laborer
45
10.7

    Student
77
18.2

    Merchant
49
11.6

Mean family size of the study participants

    1-4 individuals
146
34.6

    5-7 individuals
202
47.9

    >7 individuals
74
17.5

Estimated mean monthly family income /ETB

    ≤500
172
40.8

    501-1000
122
28.9

    >1000
51
12.1

    Unknown/no- regular income
77
18.2

8.2. Clinical Profiles of the Study Participants

In this study, 8.5% of the study participants had previous history of TB and 26.5% of them were house/bed bound because of the current illness (Table 2).

Table 2: Clinical profile of study participants among selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Frequency (N=422)
Percentage (%)

Presence of previous history of TB

    Yes
36
8.5

    No
386
91.5

Level of severity before first visit to health facility related to his daily activity

    Still do a full day work
121
28.7

    Some activity outside the house
189
44.8

    House/bed bound
112
26.5

8.3. Behavior & Knowledge Related Profiles of the Study Participants

In this study, 14.9% of the study participants were current cigarette smoker and 44.5% of the study participants had poor knowledge of tuberculosis (Table 3).

Table 3: Distribution of behavior related profiles among study participants in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Frequency (N=422)
Percentage (%)

Smoking status/behaviors of the study participants

    Never smoke
290
68.7

    Former smoker
69
16.4

    Current smoker
63
14.9

Alcoholic intake status/behaviors of the study participants

    Never drink
209
49.5

    Former drinker
130
30.8

    Current drinking
83
19.7

Knowledge score to TB

    Good
234
55.5

    Poor
188
44.5

Stigma score to TB

    No/mild
249
59.0

    Moderate
113
26.8

    Sever
60
14.2

Patient satisfaction score to healthcare system

    Good
175
41.5

    Medium
223
52.8

    Low
24
5.7

8.4. Health Accessibility & Health Seeking Behaviors of the Study Participants

Out of total study participants, 45% travel >10 Km to the nearest health facility from their home. 26.3% of the study participants visited nonformal health provider for consultation initially because of the illness. Similarly, 26.3% of the study participants visited nonformal health care provider (Table 4).

Table 4: Health accessibility & health seeking behaviors of the study participants among selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Frequency (N=422)
Percentage (%)

Home distance from the nearest health facility

    ≤10km
232
55.0

    >10km
190
45.0

Presence of other HF close to home

    Yes
175
41.5

    No
247
58.5

First health care seeking/consultation action because of the illness

    Gov.t health care provider
159
37.7

    Formal private health care provider
152
36.0

    Nonformal health care provider
111
26.3

Number healthcare providers visited because of current illness

    ≤2 healthcare providers
282
66.8

    ≥3 healthcare providers
140
33.2

Antibiotic Rx because of current illness before diagnosis made

    Yes
219
51.9

    No
203
48.1

8.5. Total Treatment Delay in TB

In this study, the median total delay in treatment of TB was 60 days (IQR: 33-81), 95% CI, 42-63. Of the total study participants, 215 (50.9%) 95% CI, 45.4-55.7 of the participants have unacceptable/longer total delay in TB treatment (delay > 60 days) (Figure 1).

Figure 1: Total treatment delay in TB.

8.6. Distribution of Total Delay in TB Treatment among Sociodemographic Characteristics

Being female gender (67.9%) among sex, age of > 45 years old (55.8%) among age group, not attending formal education (78.4%) among educational status, having rural residence (66.0%) among place of residence, and having mean family size of >7 individuals (62.2%) among mean family size of the study participants had higher unacceptable total delay in treatment of TB (Table 5).

Table 5: Distribution of total treatment delay among sociodemographic characteristics of the study participants in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Total treatment delay (≥60 days)

No (%)
Yes (%)
Total

Sex of the participants

    Male
147 (62.6)
88( 37.4)
235

    Female
60 (32.1)
127 (67.9 )
187

Age of the participants/year

    15-25
69 (52.3 )
63 ( 47.7)
132

    26-35
125 (52)
60 (48 )
125

    36-45
46( 44.2)
58 (55.8 )
104

    >45
27 ( 44.3)
34 ( 55.7)
61

Marital status of study participants

    Married
106(45.3)
128(54.7)
234

    Single
106(53.5)
128(46.5)
234

    Others
10(55.6)
8 (44.4)
18

Educational status/level

    Not attended formal education
38(21.6)
138(78.4)
176

    Primary school
99(68.8)
45(31.2)
144

    Secondary school
48 (68.6)
22(31.4)
70

    Higher education
22(68.8)
10(31.2)
32

Religion of the study participants

    Orthodox Christian
46(48.9)
48(51.1)
94

    Protestant Christian
132(48.5)
140(51.5)
272

    Muslim
29(51.8)
27(48. 2)
56

Place of residence

    Urban
123(70.3)
52(29.7)
175

    Rural
84(34.0)
163(66.0)
247

Ethnicity of the study participants

    Gedeo
120(48.6)
127(51.4)
247

    Oromo
34(41.5)
48(58.5)
82

    Amhara
20(55.6)
16(44.4)
36

    Sedamo
23(59.0)
16(41.0)
39

    Others
10(55.6)
8(44.4)
18

Occupation of the study participants

    Farmer
92 (47.2)
103(52.8)
195

    Employed
28(50.0 )
28(50.0 )
56

    Daily laborer
21(46.7 )
24(53.3 )
45

    Student
40(51.9)
37(48.1)
77

    Merchant
26(53.1)
23(46.9)
49

Mean family size of the study participants

    1-4 individuals
77(52.7)
69(47.3)
146

    5-7 individuals
102(50.5)
100(49.5)
202

28(37.8)
46 (62.2 )
74

Estimated mean monthly family income /birr

    ≤500
70(40.7)
102(59.3)
172

    501-1000
72(59 )
50( 41)
122

28(54.9)
23(45.1)
51

    Unknown/ No-regular income
37( 48.1)
40(51.9)
77

    Total
207(49.1)
215(50.9)
100%

8.7. Distribution of Total Delay in Treatment among Clinical Profiles

In this study, not taking TB treatment previously (51.8%), being house/bed bound (71.4%) had higher unacceptable total delay in treatment of TB among presence of previous history of TB & level of severity of the illness before first visit to health facility respectively (Table 6).

Table 6: Distribution of total treatment delay among clinical profiles of the study participants in selected health facilities of Gedeo Zone, southern Ethiopia, 2017/18.

Variables
Total treatment delay (≥60 days)

No (%)
Yes (%)
Total

Presence of previous history of TB

    Yes
21(58.3)
15(41.7)
36

    No
186(48.2)
200(51.8)
386

Level of severity of the illness before first visit to health facility

    Still do a full day work
72(59.5)
49(40.5)
121

    Some activity outside the house
103(54.5)
86(45.5)
189

    House/bed bound
32(28.6)
80(71.4)
112

    Total
207(49.1)
215(50.9)
100%

8.8. Distribution of Total Delay in Treatment of TB among Behavior & Knowledge Related Profiles of the Study Participants

In this study, current smoker (57.1%) among smoking status, poor knowledge of TB (64.4%), and low patient satisfaction (58.3%) among patient satisfaction to healthcare system had higher unacceptable total delay in treatment of TB (Table 7).

Table 7: Distribution of total delay in treatment among behavior & knowledge related profiles of study participants in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Total treatment delay (≥60 days)

No (%)
Yes (%)
Total

Smoking status/behaviors of the study participants

    Never smoke
146(50.3)
144(49.7)
290

    Former smoker
34(49.3)
35(50.7)
69

    Current smoker
27(42.9)
36(57.1)
63

Alcoholic intake status/behaviors of the study participants

    Never drink
102(48.8)
107 (51.2)
209

    Former drinker
67(51.5)
63(48.5)
130

    Current drinking
38(45.8)
45(54.2)
83

Knowledge to TB

    Good
140(59.8)
94(40.2)
234

    Poor
67(35.6)
121(64.4)
188

Stigma score to TB

    No/mild
132(53.0)
117(47.0)
249

    Moderate
47(41.6)
66(58.4)
113

    Sever
28(46.7)
32(53.3)
60

Patient satisfaction score to healthcare system

    Good
87(49.7)
88(50.3)
175

    Medium
110(49.3)
113(50.7)
223

    Low
10(41.7)
14(58.3)
24

    Total
207(49.1)
215(50.9)
100%

8.9. Distribution of Total Treatment Delay among Health Accessibility & Health Seeking Behaviors of the Study Participants

Having home distance >10km (69.5%) among home distance from current health facility, visiting nonformal health provider (82.0%) among first health care seeking behavior, and visiting ≥3 healthcare providers (72.9%) among number of healthcare providers visiting had higher unacceptable total delay in treatment of TB (Table 8).

Table 8: Distribution of total treatment delay among health accessibility & health seeking behaviors of the study participants in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/18.

Variables
Total treatment delay (≥60 days)

No (%)
Yes (%)
Total

Home distance from the nearest health facility

    ≤10km
149(64.2)
83(35.8)
232

    >10km
58(30.5)
132(69.5)
190

Presence of other HF close to home

    Yes
113(64.6)
62(35.4)
175

    No
94(38.1)
153(61.9)
247

First health care seeking/consultation action because of the illness

    Visited gov.t health facility
107(67.3)
52(32.7)
159

    Visited formal private health provider
80(52.6)
72(47.4)
152

    Visited nonformal health provider
20(18.0)
91(82.0)
111

Number healthcare providers visited

    ≤2 healthcare providers
169(59.9)
113(40.1)
282

    ≥3 healthcare providers
38(27.1)
102(72.9)
140

Antibiotic Rx because of current illness before diagnosis

    Yes
78(35.6)
141(64.4)
219

    No
129(63.5)
74(36.5)
203

    Total
207(49.1)
215(50.9)
100%

8.10. Bivariate and Multivariate Analysis of Associated Factors for Longer Total Treatment Delay

In univariate analysis, sex, education status, residency, family size, marital status of study participants, monthly family income, level of severity before first visit to health facility, presence of previous history of TB, stigma, knowledge of TB, home distance from the nearest health facility, presence of other health facilities close to home, first health care seeking behavior, number of healthcare providers visiting and presence of antibiotic treatment because of current illness had p<0.25 which was eligible for multivariate analysis.

In multivariate analysis, after adjusting the eligible variable, only being of female gender, not attending formal education, having rural residency, having poor knowledge of TB, having home distance >10km from the nearest health facility, visiting nonformal health care provider, and taking antibiotic treatment because of current illness was identified as independently associated risk factors for unacceptable total delay in treatment of TB as presented in Table 9.

Table 9: Bivariate and multivariate analysis of associated factors for total treatment delay among study participants of selected health facilities of Gedeo Zone, southern Ethiopia, 2017/18.

Variables
Total treatment delay
(≥ 60 days)
Bivariate
Multivariate

No (%)
Yes (%)
Total
COR (95% CI)
P- value
AOR (95% CI)
P- value

Sex of the participants
0.001

0.001

    Male
147(62.6)
88( 37.4)
235
1

1

    Female
60 (32.1)
127 (67.9 )
187
3.5(2.3-5.3)
0.001
2.6(1.5-4.5)
0.001

Age of the participants/ year
0 .475

    15-25
69 (52.3 )
63 ( 47.7)
132
0.9(0.6-1.6)
0.965

    26-35
125 (52)
60 (48 )
125
1

    36-45
46( 44.2)
58 (55.8 )
104
1.4(0.8-2.3)
0.242

    >45
27 ( 44.3)
34 ( 55.7)
61
1.4(0.7-2.5)
0.322

Marital status of study participants
0.225

    Married
106(45.3)
128(54.7)
234
1

    Single
106(53.5)
128(46.5)
234
0.7(0.5-1.0)
0.103

    Others
10(55.6)
8 (44.4)
18
0.7(0.3-1.7)
0.403

Educational status/level

0.001

0.001

    Not attended formal education
38(21.6)
138(78.4)
176
7.9(3.5-18.3)
0.001
7.0(2.5-19.7)
0.001

    Primary school
99(68.8)
45(31.2)
144
1.0(0.4-2.3)
1.000
1.1(0.4-2.9)
0.891

    Secondary school
48 (68.6)
22(31.4)
70
1.0(0.4-2.5)
0.986
1.2(0.4    3.5)
0.774

    Higher education
22(68.8)
10(31.2)
32
1

1

Religion of the study participants
0.906

Orthodox Christian
46(48.9)
48(51.1)
94
1.1(0.6-2.1)
0.736

Protestant Christian
132(48.5)
140(51.5)
272
1.1(0.6-2.0)
0.657

Muslim
29(51.8)
27(48. 2)
56
1

Place of residence

0.001

0.013

    Urban
123(70.3)
52(29.7)
175
1

1

    Rural
84(34.0)
163(66.0)
247
4.5(3.0-6.9)
0.001
2.0(1.2    3.5)
0.013

Ethnicity of the study participants

0.364

    Gedeo
120(48.6)
127(51.4)
247
1.3(0.5-3.5)
0.569

    Oromo
34(41.5)
48(58.5)
82
1.7(0.6-4.9)
0.279

    Amhara
20(55.6)
16(44.4)
36
1.0(0.3-3.1)
1.000

    Sedama
23(59.0)
16(41.0)
39
0.8(0.3-2.7)
0.808

    Others
10(55.6)
8(44.4)
18
1

Occupation of the study participants
0.915

    Farmer
92 (47.2)
103(52.8)
195
1.3(0.7-2.4)
0.462

    Employed
28(50.0 )
28(50.0 )
56
1.2(0.5-2.4)
0.754

    Daily laborer
21(46.7 )
24(53.3 )
45
1.3(0.6-2.9)
0.536

    Student
40(51.9)
37(48.1)
77
1.1(0.5-2.1)
0.903

    Merchant
26(53.1)
23(46.9)
49
1

Mean family size of the study participants
0.099

    1-4 individuals
77(52.7)
69(47.3)
146
1

1
0.705

    5-7 individuals
102(50.5)
100(49.5)
202
1.1(0.7-1.7)
0.679
1.2(0.7-2.2)
0.482

    >7 individuals
28(37.8)
46 (62.2 )
74
1.8(1.0-3.2)
0.038
1.3(0.6-2.9)
0.481

Estimated mean monthly family income/birr
0.016

0.929

    ≤500
70(40.7)
102(59.3)
172
1.8(0.9-3.3)
0.074
1.1(0.4    2.9)
0.783

    501-1000
72(59 )
50( 41)
122
0.8(0.4-1.6)
0.618
0.9(0.4-2.5)
0.926

    >1000
28(54.9)
23(45.1)
51
1

1

    Unknown/ No- regular income
37( 48.1)
40(51.9)
77
1.3(0.6-2.7)
0.448
0.9(0.3-2.7)
0.853

Presence of previous history of TB
0.247

    Yes
21(58.3)
15(41.7)
36
1

    No
186(48.2)
200(51.8)
386
1.5(0.7-3.0)
0.247

Level of severity before first visit to health facility
0.001

0.379

    Still do a full day work
72(59.5)
49(40.5)
121
1

1

    Some activity outside the house
103(54.5)
86(45.5)
189
1.2(0.8-1.9)
0.386
1.4(0.7-2.6)
0.311

    House/bed bound
32(28.6)
80(71.4)
112
3.7(2.1-6.3)
0.001
1.7(0.8    3.7)
0.174

Smoking status/behaviors of the participants

0.561

    Never smoke
146(50.3)
144(49.7)
290
1

    Former smoker
34(49.3)
35(50.7)
69
1.3(0.8    2.3)
0.282

    Current smoker
27(42.9)
36(57.1)
63
1.1(0.6-1.7)
0.873

Alcoholic intake status/behaviors of the study participants
0.711

    Never drink
102(48.8)
107(51.2)
209
1

    Former drinker
67(51.5)
63(48.5)
130
1.1(0.7-1.8)
0.641

    Current drinking
38(45.8)
45(54.2)
83
0.9(0.6-1.4)
0.624

Knowledge score to TB

0.001

0.038

    Good
140(59.8)
94(40.2)
234
1

1

    Poor
67(35.6)
121(64.4)
188
2.7(1.8-3.9)
0.001
1.8(1.0-3.2)
0.038

Stigma score to TB

0.123

0.931

    No/mild
132(53.0)
117(47.0)
249
1

1

    Moderate
47(41.6)
66(58.4)
113
1.6(1.0-2.5)
0.045
0.9(0.5    1.8)
0.862

    Sever
28(46.7)
32(53.3)
60
1.3(0.7-2.3)
0.378
0.8(0.4    1.9)
0.714

Patient satisfaction score to healthcare system
0.757

    Good
87(49.7)
88(50.3)
175
1

    Medium
110(49.3)
113(50.7)
223
1.0(0.7-1.5)
0.939

    Sever
10(41.7)
14(58.3)
24
1.4(0.6-3.3)
0.461

Home distance from the nearest health facility
0.001

0.005

    ≤10km
149(64.2)
83(35.8)
232
1

1

    >10km
58(30.5)
132(69.5)
190
4.1(2.7-6.1)
0.001
2.2(1.3-3.7)
0.005

Presence of other HF close to home
0.001

0.123

    Yes
113(64.6)
62(35.4)
175
1

    No
94(38.1)
153(61.9)
247
2.9(1.9-4.4)
0.001
1.5(0.9-2.7)
0.123

First health care consultation action because of the illness
0.001

0.002

    Gov.t health facility
107(67.3)
52(32.7)
159
1

1

    Formal private health provider
80(52.6)
72(47.4)
152
1.8(1.2- 2.9)
0.009
1.6(0.9-2.9)
0.082

    Nonformal health provider
20(18.0)
91(82.0)
111
9.4(5.2-16.8)
0.001
3.8(1.8-7.9)
0.001

Number healthcare providers visited
0.001

0.184

    ≤2 providers
169(59.9)
113(40.1)
282
1

1

    ≥3 providers
38(27.1)
102(72.9)
140
4.0(2.6-6.2)
0.001
1.5(0.8-2.9)
0.184

Antibiotic Rx because of current illness

0.001

0.001

    Yes
78(35.6)
141(64.4)
219
3.1(2.1- 4.7)
0.001
6.5(3.6-11.7)
0.001

    No
129(63.5)
74(36.5)
203
1

1

Keys: P value ≤ 0.25 in bivariate analysis, P value ≤ 0.05 in multivariate analysis and its significantly independent associated factors.

9. Discussion

Early diagnosis and initiation of treatment is a determining factor for spread and infectivity of TB. This may worsen the disease and cause higher mortality which is still prevailing problem around the globe especially in resource-limited countries [2, 3, 6, 17]. The present study focuses on assessing the total delay in TB treatment & associated factors among patients with pulmonary tuberculosis. Variations of total delay in treatment of TB were reported from setting to setting across countries because of geographical, economic, and cultural variations to access TB diagnosis and treatment service [3, 18]. This study identified that median total delay in treatment of TB was 60 days (95% CI, 42-63). This is consistent with a study done in Uzbekistan [11]; Southern Ethiopia [25]; Northwest Ethiopia [16]; and West Gojjam, Ethiopia [17], with a median total treatment delay of 50 days, 45 days, 60 days, and 60 days, respectively.

This finding is higher than that of study done in India [15]; Uganda [12]; Nepal [19]; Arsi Zone, Ethiopia [20]; and Arbaminch, Ethiopia [21], with a median total treatment delay of 36 days, 28 days, 39.5 days, 40 days, and 35 days, respectively. This difference may be due to socioeconomical difference of access to TB care (available diagnostic facilities), inclusion/exclusion criteria, and sample size. Another reason might be difference in study area/population difference (health seeking behavior, knowledge and attitude of the participants).

This finding is lower than that of study done in Ghana [22]; Guinea-Bissau [6]; Italy [23]; Ahvaz [24], Bale Zone Ethiopia [14]; East Wollega, Ethiopia [26]; Amhara region, Ethiopia [27]; Afar region, Ethiopia [28], with a median total treatment delay of 104 days, 84.7 days, 77.5 days, 73 day, 97 days, 90 days, 80 days, and 70.5 days, respectively. This difference may be due to difference in access to TB care (available diagnostic facilities), inclusion/exclusion criteria, sample size, study area/population difference (health seeking behavior, knowledge, and attitude of the participants), and study period (improvement in diagnosis, treatment, and monitoring services considerably in the last five years may improve the delay in treatment. This might be due to expansions of DOTS services, which made better accessibility in seeking health care for TB treatments compared to the previous study). Another possible reason might be that this study includes some urban and most rural health facilities compared to a solely rural setting in Guinea-Bissau [6].

In the present study, it was found that there was an overall 50.9% (95% CI, 45.4-55.7) prevalence of unacceptable total delay in treatment of TB. This observed result is in line with a previous study in Uzbekistan [11]; Arsi Zone, Ethiopia [20]; Southern Ethiopia [25]; Afar region [28]; Arbaminch, Ethiopia [21]; and West Gojjam, Ethiopia [17], with 50%, 48.9%, 49%, 50%, 46%, and 50% of patients with observed unacceptable delay, respectively.

This finding is higher than that of a study done in India [15] with 29% of patients with observed unacceptable delay. However, it is lower than study done in Ghana [22], Uganda [12], and Nepal [19], with 82.2 %, 91%, and 62.8 % of patients with observed unacceptable delay, respectively. This discrepancy might be due to differences in sample size, study setting, and dichotomization of cut-off points of total treatment delay as cut-off points to determine delays.

Understanding the factors associated with patient delays is vital for the achievement of reduction in TB morbidity and mortality. Studies conducted in different countries have shown that many factors are involved in delayed treatment of tuberculosis patients [3, 10, 29]. In the study, being of female gender was identified as independent associated factor for development of unacceptable total delay in treatment of TB than their counterparts. This is similar with study in Ahvaz [24], Nigeria [13], Uganda [12], and Southern Ethiopia [25]. This may be due to the fact that socioeconomic and cultural position of women may influence their opportunities and add constraints to healthcare access and needs [30]. This may be explained by limited decision making power, engagement in domestic work, unemployment, and facility too far in study area [30–32].

Regarding educational status, not attending formal education was reported as associated factor for development of unacceptable total delay in treatment of TB in this study. This is in line with study done in Guinea-Bissau [6], Mediterranean region, Egypt [3], and Ethiopia [33]. This could be due to the fact that those attending tertiary education might have better information about TB, increased awareness of the TB disease, and being reinforced by good treatment seeking behavior and may likely seek care early [34]

Having rural residency among the study participants was also reported as associated factor for unacceptable total delay in treatment of TB development in this study. This is similar with study done in Mediterranean region, Pakistan and Somalia [3], Nigeria [13], and three studies from Ethiopia (10 DOTS districts of Ethiopia [33], North Wollo zone [35], and Arbaminch [21]). This may be explained such that rural residency may limit the study participants to have appropriate access to health information and health facilities than the urban residency. In rural residency they may have lack of supervision of health staff to provide health information at peripheral level resulting in low education level of TB than urban areas [34]. This may predispose the individual to have poorer access to health care in rural areas. This is because of the fact that rural residency may make it difficult for the participants to travel to health facility in terms of travel time from patient’s areas of residences to public facilities which is closely related to income level [34, 36, 37].

Moreover, home distance to travel > 10 km to reach the nearest public health facility was also reported as causing unacceptable delay in TB treatment development. This finding is consistent with study in Mediterranean region, Egypt and Yemen [3], Nigeria [38], Bale Zone, and Ethiopia [14]. This may be because the facility is too far from the study participant’s home which may limit access to health care in terms of travel time from patients' areas of residences to public health facilities [37, 39]. This may result in low accessibility in health service & delay in seeking health care of TB treatments.

Furthermore, health care seeking behaviors of the respondents were documented for unacceptable treatment delay in TB in this study. Visiting nonformal health provider was identified as associated factor for development of unacceptable total delay in treatment of TB. This is in line with study in Uzbekistan [11], India [15], Mozambque [38], Afar, Ethiopia [28], Mediterranean region, Somalia [3], three studies from Ethiopia (Amhara region [27], West Gojjam [17], North and Wollo zone [35], Bale Zone, Ethiopia [14]). This might cause low reliance of treatments in health facility and strong cultural bond in holy water and traditional healer treatments leading the respondents to seek care for TB treatments after failure of treatments in informal sources [40].

With respect to knowledge of the study participants, this study revealed that having poor knowledge of TB is an associated factor in development of unacceptable total delay in treatment of TB. This finding is consistent with study documented in Mediterranean region, Pakistan [3], India [15], Mozambque [38], North Wollo, Ethiopia [35], and West Gojjam, Ethiopia [17]. This might be due to study participants with good knowledge about TB might have better inclination for early seeking of medical care. This means having good knowledge of tuberculosis means of transmission, prevention diagnosis & treatment option are vital for early seeking of TB medical care.

Prior unspecific treatment before diagnosis of the current illness was identified as associated factor for delay in TB treatment in this study. Similar studies were reported in Italy [23]. Patients receiving antibiotics prior to TB confirmation experience a process-related delay in starting treatment. This empirical antibiotic treatment may lower some sign/symptoms of TB which will make the patient delay to request diagnosis & treatment [41]. For example, fluoroquinolones treatment was found to be effective in lower respiratory symptoms of TB and initial results usually improvement. This may suggest the delay was due to the time inherent in taking a course of antibiotics and waiting to see if there is a clinical response [42, 43].

10. Limitations of the Study

(i)The design of our study unfortunately did not outline to identify factors such as antibiotic treatment (the prescriber/source of the drug, type drug & duration).(ii)This study lacks standard cut-off point for unacceptable total treatment delay and we used the cut of point as the median of the total treatment delay.(iii)Furthermore, information for this study relied on the participants self-reported duration of total delay and therefore it may be subject to recall bias.

11. Conclusions

It revealed that there is still a high median total delay (60 days) with an overall high prevalence of unacceptable/longer total delay of 50.9%. Female gender, rural residence, not attending formal education, visiting nonformal health facility as first health care seeking, having poor knowledge of TB & having antibiotic treatment before the current TB diagnosis were identified as independent associated factors for unacceptable total delay in treatment of TB.

12. Recommendations

Woreda, Zonal & other health stakeholders office collaborative work should be developed to further decentralization of TB diagnostic and treatment facilities to the periphery to increase & expand health care accessibility (TB diagnosis & treatment service) among people living in rural areas, especially among females in all areas.

(1)Tuberculosis control programmes in similar settings should consider innovative strategies for TB education, advocacy, communication, and social mobilization to the rural area & female gender.(2)Due attention should be given to increase public awareness & health education about the symptoms of tuberculosis, the availability and location of free diagnostic services & seeking early care and treatment of TB with designing health education directed towards how to suspect and recognize TB symptoms and the importance of early health seeking.(3)Woreda, Zonal & other health stakeholders offices should give emphasis to collaborate with informal health care provider (traditional healers, local drug sellers, traditional healers, and religious leaders) to design training & discussion on how to suspect TB symptoms & the way to refer early to government health facilities for diagnosis.(4)Woreda, Zonal & other educational stakeholders should work on to increase & expand accessibility of formal education to the community for early diagnosis & treatment of TB.(5)The duration of total delay and the significant factors of the delay identified in the present study should be incorporated into routine TB surveillance report protocol.(6)Physicians should exert efforts to minimise prior antibiotic treatment of respiratory tract infection by including TB in their differential diagnosis and initiate simple, rapid relevant TB-focused diagnostic investigations early on in the diagnostic process to quickly exclude M. tuberculosis in the management of respiratory tract infection.(7)Further nationwide and extensive surveillance on duration of total delay and the significant factors of the delay should be done to design & develop programme alternative diagnosis & prevention, & treatment strategies.

Data Availability

The “data collection Questionnaire” data used to support the findings of this study are included within the supplementary information file.

Disclosure

All authors were involved in the work and shaped this manuscript writing without the influence of supporting institution. The funder is not involved in the manuscript writing, editing, approval, or decision to publish.

Conflicts of Interest

Authors declare that there are no conflicts of interest regarding the publication of this paper.

Acknowledgments

We would like to thanks study participants for providing necessary information for the finding. Furthermore, we want to acknowledge data collectors & respective study site health facility leaders for their help for data collection process. We would like to thank College of Health Science & Medicine for financial support of this research.

Supplementary Materials

Questionnaire to assessment of total delay in treatment of TB and associated factors among new pulmonary TB patients in selected health facilities of Gedeo Zone, Southern Ethiopia, 2017/1. (Supplementary Materials)

References

A. Nancy and R. Knechel, “Tuberculosis: pathophysiology, clinical features, and diagnosis,” Critical Care Nurse, vol. 29, no. 2, pp. 34–44, 2009.

World Health Organization/WHO, Global Tuberculosis Report 2016, World Health Organization/WHO, 2017.

World Health Organization/WHO, Diagnostic and Treatment Delay in Tuberculosis: An in-Depth Analysis of the Health-Seeking Behavior of Patients and Health System Response in Seven Countries of the Eastern Mediterranean Region, 2006.

USAID, International standards for Tuberclosis Care, 3rd edition, 2014.

R. L. Serafino, W. Mbbs, and T. Med, “Clinical manifestations of pulmonary and extra-pulmonary tuberculosis,” South Sudan Medical Journal, vol. 6, no. 3, pp. 52–56, 2013.

J. Virenfeldt, F. Rudolf, C. Camara et al., “Treatment delay affects clinical severity of tuberculosis: A longitudinal cohort study,” BMJ Open, vol. 4, no. 6, Article ID e004818, 2014.

D. G. Storla, S. Yimer, and G. A. Bjune, “Delay in the diagnosis and treatment of tuberculosis,” BMC Public Health, vol. 9, pp. 1–9, 2008.

International Standards for Tuberclosis Care (ISTC), Tuberculosis Care Coalition for Technical Assistance, 2006.

I. In and T. Forward, “Why TB ? evaluating the national TB control program : challenges and ways forward,” in Proceedings of the Federal Ministry of Health 16 th National Annual Review Meeting Group Discussion, pp. 16–21, Disease Prevention and Control Directorate, 2014.

Y. Li, J. Ehiri, S. Tang et al., “Factors associated with patient, and diagnostic delays in Chinese TB patients: a systematic review and meta-analysis,” BMC Medicine, vol. 11, article 156, 2013.

T. V. Belkina, D. S. Khojiev, M. N. Tillyashaykhov et al., “Delay in the diagnosis and treatment of pulmonary tuberculosis in Uzbekistan: a cross-sectional study,” BMC Infectious Diseases, vol. 14, no. 1, pp. 1–8, 2014.

E. Buregyeya, B. Criel, F. Nuwaha, and R. Colebunders, “Delays in diagnosis and treatment of pulmonary tuberculosis in Wakiso and Mukono districts, Uganda,” BMC Public Health, vol. 14, no. 1, pp. 1–10, 2014.

A. A. Fatiregun and C. C. Ejeckam, “Determinants of patient delay in seeking treatment among pulmonary tuberculosis cases in a government specialist hospital in Ibadan, Nigeria,” Tanzania Journal of Health Research, vol. 12, no. 2, 2010.

A. Hussen, S. Biadgilign, F. Tessema, S. Mohammed, K. Deribe, and A. Deribew, “Treatment delay among pulmonary tuberculosis patients in pastoralist communities in Bale Zone, Southeast Ethiopia,” BMC Research Notes, vol. 5, 2012.

U. R. Mandi and H. Pradesh, Delay in Diagnosis and Treatment among TB Patients Registered, 2012.

S. A. Yimer, G. A. Bjune, and C. Holm-Hansen, “Time to first consultation, diagnosis and treatment of TB among patients attending a referral hospital in Northwest, Ethiopia,” BMC Infectious Diseases, vol. 14, no. 19, 2014.

S. B. Gebreegziabher, G. A. Bjune, and S. A. Yimer, “Total delay is associated with unfavorable treatment outcome among pulmonary tuberculosis patients in West Gojjam Zone, Northwest Ethiopia: A prospective cohort study,” PLoS ONE, vol. 11, no. 7, Article ID e0159579, 2016.

C. T. Sreeramareddy, Z. Z. Qin, S. Satyanarayana, S. Ramnath, and M. Pai, “Delays in diagnosis and treatment of pulmonary tuberculosis in India,” International Journal of Tuberculosis and Lung Disease, vol. 18, no. 3, pp. 255–266, 2014.

R. K. Mahato, W. Laohasiriwong, K. Vaeteewootacharn, R. Koju, and R. Bhattarai, “Major delays in the diagnosis and management of tuberculosis patients in Nepal,” Journal of Clinical and Diagnostic Research, vol. 9, no. 10, pp. 5–9, 2015.

A. Hamza, M. Demissie, S. Gare, and G. Teshome, “Delay in tuberculosis diagnosis among tuberculosis patients at the three hospitals: asella, robe and abomsa of arsi zone, oromia regional state, March, 2015,” OALib, vol. 2, no. 12, pp. 1–13, 2015.

Z. Z. Zeleke and Z. M. Trifa, “Treatment delay among smear positive pulmonary tuberculosis patients in South Ethiopia: a cross-sectional study,” Science Journal of Public Health, vol. 2, no. 5, pp. 402–409, 2014.

E. Osei, P. Akweongo, and F. Binka, “Factors associated with DELAY in diagnosis among tuberculosis patients in Hohoe Municipality, Ghana,” BMC Public Health, vol. 15, no. 1, pp. 1–11, 2015.

P. Pezzotti, S. Pozzato, E. Ferroni et al., “Delay in diagnosis of pulmonary tuberculosis: a survey in the Lazio region, Italy,” Epidemiology, Biostatistics and Public Health, vol. 12, no. 1, pp. 94941–94950, 2015.

S. M. Alavi, P. Bakhtiyariniya, and A. Albagi, “Factors associated with delay in diagnosis and treatment of pulmonary tuberculosis,” Jundishapur Journal of Microbiology, vol. 8, no. 3, pp. 8–11, 2015.

A. Asefa and W. Teshome, “Total delay in treatment among smear positive pulmonary tuberculosis patients in five primary health centers, Southern Ethiopia: a cross sectional study,” PLoS ONE, vol. 9, no. 7, Article ID e102884, 2014.

T. Wondimu, K. W. Michael, W. Kassahun, and S. Getachew, “Delay in initiating tuberculosis treatment and factors associated among pulmonary tuberculosis patients in East Wollega, Western Ethiopia,” Ethiopian Journal of Health Development, vol. 21, no. 2, pp. 148–156, 2007.

S. Yimer, G. Bjune, and G. Alene, “Diagnostic and treatment delay among pulmonary tuberculosis patients in Ethiopia: a cross sectional study,” BMC Infectious Diseases, vol. 5, article 112, pp. 1–7, 2005.

M. Belay, G. Bjune, G. Ameni, and F. Abebe, “Diagnostic and treatment delay among Tuberculosis patients in Afar Region, Ethiopia: a cross-sectional study,” BMC Public Health, vol. 12, no. 1, article 369, 2012.

USAID, Barriers to Access and Use of Public TB Diagnostic Services in Vietnam, 2013.

Z. Mumtaz, S. Salway, M. Waseem, and N. Umer, “Gender-based barriers to primary health care provision in Pakistan: the experience of female providers,” Health Policy and Planning, vol. 18, no. 3, pp. 261–269, 2003.

C. R. Gounder, T. Akande, W. D. Neve et al., “Barriers and delays in tuberculosis diagnosis and treatment services : does gender matter ?” Citation Diagnosis and Treatment Se, 2016.

The partnership for Maternal Newborn & Child Health, “Promoting women’s empowerment for better health outcpmes for women and children,” in Partner in Population & Development, pp. 1–4, Beijing, China, 2013.

M. M. Mesfin, J. N. Newell, J. D. Walley, A. Gessessew, and R. J. Madeley, “Delayed consultation among pulmonary tuberculosis patients: a cross sectional study of 10 DOTS districts of Ethiopia,” BMC Public Health, vol. 9, pp. 1–10, 2009.

F. Ahmad, T. A. Pakasi, and M. Mansyur, “The social determinants of knowledge and perception on pulmonary tuberculosis among females in Jakarta, Indonesia,” Medical Journal of Indonesia, vol. 23, no. 2, Article ID 614043689, pp. 93–105, 2014.

D. Tsegaye, E. Abiy, T. Mesele, and T. Tadesse, “Delay in seeking health care and associated factors among pulmonary tuberculosis patients in north Wollo Zone, Northeast Ethiopia: institution based cross-sectional study,” Archives of Clinical Microbiology, pp. 1–7, 2016.

M. N. Mondal, H. M. Nazrul, M. R. K. Chowdhury, and J. Howard, “Socio-demographic factors affecting knowledge level of tuberculosis patients in Rajshahi city, Bangladesh,” African Health Sciences, vol. 14, no. 4, pp. 855–865, 2014.

T. Awoyemi, O. Obayelu, and H. Opaluwa, “Effect of distance on utilization of health care services in rural kogi state, Nigeria,” Journal of Human Ecology, vol. 35, no. 1, pp. 1–9, 2011.

A. Saifodine, P. S. Gudo, M. Sidat, and J. Black, “Patient and health system delay among patients with pulmonary tuberculosis in Beira city, Mozambique,” BMC Public Health, vol. 13, no. 1, 2013.

T. E. Ursulica, “The relationship between health care needs and accessibility to health care services in botosani county- Romania,” Procedia Environmental Sciences, vol. 32, pp. 300–310, 2016.

M. Colvin, L. Gumede, K. Grimwade, D. Maher, and D. Wilkinson, “Contribution of traditional healers to a rural tuberculosis control programme in Hlabisa, South Africa,” The International Journal of Tuberculosis and Lung Disease, vol. 7, no. 9, pp. S86–S91, 2003.

K. E. Dooley, J. Golub, F. S. Goes, W. G. Merz, and T. R. Sterling, “Empiric treatment of community-acquired pneumonia with fluoroquinolones, and delays in the treatment of tuberculosis,” Clinical Infectious Diseases, vol. 34, no. 12, pp. 1607–1612, 2002.

T.-C. Chen, P.-L. Lu, C.-Y. Lin, W.-R. Lin, and Y.-H. Chen, “Fluoroquinolones are associated with delayed treatment and resistance in tuberculosis: a systematic review and meta-analysis,” International Journal of Infectious Diseases, vol. 15, no. 3, pp. e211–e216, 2011.

S. E. Craig, H. Bettinson, C. A. Sabin, and L. M. Gillespie, “Think TB! is the diagnosis of pulmonary tuberculosis delayed by the use of antibiotics?” International Journal of Tuberculosis and Lung Disease, vol. 13, no. 2, pp. 208–13, 2009.