Background
Interest to eliminate tuberculosis (TB) transmission in health facilities is growing in importance because of the association between TB and HIV and the emergence of multidrug resistant TB (MDR-TB) and extensively drug-resistant TB (XDR-TB) [
1]. HIV is a risk factor for developing TB. In addition to reactivating latent
Mycobacterium Tuberculosis (MTB) infection [
2], HIV increases the risk of rapid TB progression after infection or re-infection with MTB [
3,
4]. Moreover, the risk of TB transmission in health facilities from individuals with TB to other patients and health care workers (HCWs), causing substantial morbidity and mortality is well documented [
5‐
7]. The risk of nosocomial transmission of TB is high in sub-Saharan Africa, where TB and HIV prevalence are high [
6,
8,
9]. This risk is greater when larger numbers of infectious (smear-positive) TB patients are managed at health-care facilities, that don’t have effective infection-control measures [
1,
10]. The situation is worsened by the increasing number of patients without corresponding infrastructure expansion and health care worker (HCW) recruitment, leading to overcrowding of patients, delayed diagnosis and treatment resulting into increased TB transmission [
11]. In addition, challenges such as the impact of dual TB and HIV epidemic and the increasing TB drug resistant cases (M/X/DR-TB) [
6,
9,
12,
13] have stimulated the need for strengthening the TB prevention and control in health facilities as well in community settings.
The World Health Organization (WHO) recommends four types of infection control measures in health facilities: managerial measures, administrative measures, proper ventilation and personal protective equipment [
14]. These measures have been found to minimize the transmission of TB in health facilities [
15,
16]. WHO therefore recommends that all health facilities caring for TB patients or persons suspected of having TB implement these measures [
1]. Previous research has found that although TBIC guidelines are available for resource-limited settings, their implementation is inadequate [
17]. In addition, it has also been found that HCWs often lack knowledge about TB and infection control [
18]. Moreover, infection control measures are often not implemented even when HCWs are well informed [
19‐
24]. Lately, the Ministry of Health of Uganda (MOH) and the Tuberculosis Control Assistance Programme (TBCAP) initiated efforts to implement TBIC by training HCWs. However, the extent to which TBIC measures have been implemented in district health facilities has not been evaluated. HIV prevalence in Uganda is high, at 7.3% among adults aged 15–49 years. Uganda ranks 20 among 22 countries with a high burden of TB; 54% of TB patients are HIV co-infected and about 30% of the HIV-related deaths are attributed to TB [
25]. In 2010, MDR-TB posed a problem in 1.1% of new cases and 12% of retreatment cases [
13]. In addition, Uganda has a case detection rate of 61%, a treatment success rate of 68% and a treatment failure rate of 10% [
25]. This calls for an assessment of TBIC measures in health facilities in Uganda. To our knowledge no study has looked at the implementation of TBIC measures in health facilities. Therefore, the purpose of this study was to assess the implementation of TBIC in health facilities in Mukono and Wakiso districts. In addition, we determined whether facility characteristics were associated with implementation of TBIC and identified barriers to implementation.
Results
More than half (65%) of the facilities were HCIIIs. Most facilities (80%) were government owned, Table
1. The median annual patient load/patient encounters in outpatient clinics was 16,212 (IQR 11,500-22,496). The median number of TB patients seen/diagnosed in the facilities annually was 24. Almost a quarter of the facilities did not have TB diagnostic facilities on site.
Table 1
General characteristics of health facilities in Mukono and Wakiso districts
Number of facilities
| | |
Mukono district | 21 | 41.2 |
Wakiso district | 30 | 58.8 |
Facility level
| | |
Hospital | 10 | 19.6 |
HC IV | 8 | 15.7 |
HC III | 33 | 64.7 |
Facility ownership
| | |
Government | 41 | 80.4 |
Private-Not-For-Profit | 10 | 19.6 |
Outpatient turnover per year
| | |
Median | 16,212 (IQR 11,500-22,496) | - |
TB patient turnover per year
| | |
Median | 24 (IQR 12–61) | - |
Staffing at health facilities
| | |
Median | 12 (IQR10-25) | - |
TB diagnosis
| | |
On-site | 39 | 76.5 |
Off-site (requires referral) | 12 | 23.5 |
TB infection control measures in the facilities
Facility level managerial measures
Availability of TBIC plan
Only 16/51 (31%) facilities had a TB infection control plan. Facilities which reported training their staff in TBIC were more likely to have a TBIC plan. However, facility level and ownership were not associated with having a TBIC plan, (Table
2). In a multivariable model, facilities from Mukono district were more likely to have TBIC plan than those of Wakiso (adjusted Odds Ratio [aOR] = 34.9 (5.9-204.7).
Table 2
Facility characteristics associated with availability of a TB infection plan in health facilities in Mukono and Wakiso districts
District
| | | | |
Wakiso | 2/30 (6.7%) | 1 | 1 | |
Mukono | 15/21 (71.0%) | 35 (6.3-195.2) | 34.9 (5.9-204.7) | <0.01 |
Facility level* | | | | |
Primary | 9/33 (27.3%) | 1 | 1 | |
Tertiary | 8/18 (44.4%) | 2.1 (0.64-7.1) | 2.1 (0.25-18.5) | 0.49 |
Ownership
| | | | |
PNFP | 5/10 (50%) | 1 | 1 | |
Government | 12/41 (29.3%) | 0.41 (0.101-1.7) | 1.2 (0.91-14.8) | 0.91 |
Staff training in TB IC
| | | | |
No | 0/16 (0%) | | | |
Yes | 17/35 (48.6%) | | | |
Staff numbers
(
quartiles
)
| | | | |
>9 | 2/10 (20.0%) | 1 | - | - |
10-11 | 1/11 (9.1%) | 0.4 (0.03-5.24) | | |
12-24 | 3/12 (25.0%) | 1.3 (0.17-10.1) | | |
25-118 | 7/13 (53.9%) | 4.7 (0.70-31.0) | | |
Administrative measures
Screening of TB suspects
At the outpatient’s departments, less than half of the facilities (22/51; 43%) reported screening patients for cough as they enter the facility, Table
3. However, direct observation showed that 46/51 (90%) of the facilities did not screen patients at all, only three facilities occasionally screened while two facilities always screened patients. Facilities from Mukono districts were more likely to report screening patients for cough than those from Wakiso (OR=2.7; 95% CI= 0.84-8.42), although the difference was not statistically significant. Facilities with high patient load were more likely to screen than those with few patients; (Table
4). Facility level, ownership, staff numbers in the facility and report of staff training in TBIC were not associated with observed patient screening. In a multivariable model, facilities from Mukono districts were more likely to report screening of patients for cough (aOR= 6.2; 95% CI= 1.10-34.58). No factors were associated with observed (always and occasionally) patient screening for cough in outpatient departments.
Table 3
Observed and reported administrative measures in facilities enhancing TB infection control in Mukono and Wakiso districts
1. Patients screened for cough as they enter the facility | Yes | 5 | 9.8 | 22 | 43.1 | 0.08 |
2. TB suspects fast tracked (triaged) | Yes | 4 | 7.8 | 25 | 49 | 0.03* |
3. TB suspects separated from other patients | Yes | 5 | 10 | 28 | 55 | 0.03* |
4. TB suspects provided with masks | Yes | 0 | | 2 | 96 | - |
5. Designated & well ventilated area for sputum collection | Yes | - | - | 16/38 | 42 | - |
Table 4
Facility characteristics associated with reported patient screening for cough in Mukono and Wakiso health facilities
District
| | | | |
Wakiso | 10/30 (33.3%) | 1 | 1 | |
Mukono | 12/21 (57.1%) | 2.7 (0.84-8.42) | 6.2 (1.10-34.58) | 0.04 |
Facility level
| | | | |
Primary | 12/33 (36.4%) | 1 | 1 | |
Tertiary | 10/18 (55.6%) | 2.2 (0.68-7.0) | 0.2 (0.01-2.70) | 0.21 |
Ownership
| | | | |
PNFP | 5/10 (50.0%) | 1 | | |
Government | 17/41 (41.5%) | 0.71 (0.17-2.83) | - | - |
Staff training in TB IC
| | | | |
No | 0/16 (0.0%) | - | | |
Yes | 22/35 (62.9%) | | | |
Staff numbers
(
quartiles
)
| | | | |
>9 | 3/10 (30.0%) | 1 | 1 | |
10-11 | 2/11 (18.2%) | 0.5 (0.7-4.0) | 1.0 (0.92-11.28) | 0.92 |
12-24 | 8/12 (66.7%) | 4.7 (0.8-28.5) | 4.9 (0.37-64.33) | 0.23 |
25-118 | 8/13 (61.5%) | 3.7 (0.6-21.6) | 7.80 (0.27-225-78) | 0.23 |
Annual outpatient turnover
(
quartiles
)
| | | | |
<8499 | 1/11 (9.1%) | 1 | 1 | |
8,500-17,999 | 5/11 (45.5%) | 8.3 (0.78-89.5) | 4.2 (0.29-59.98) | 0.29 |
18,000-66,442 | 6/11 (54.5%) | 12 (1.1-128.8) | 9.5 (0.70-127.89) | 0.09 |
>66,443 | 8/12 (66.7%) | 20 (1.85-216.2) | 19.6 (1.05-366.79) | 0.05 |
Other administrative measures
Coughing patients were not given priority in outpatients departments in over 90% (47/51) of the facilities (Table
3). They were observed waiting in the same area with other patients for long hours in queues. Only two facilities reported providing masks/tissues to coughing patients, with one facility observed giving them only to confirmed TB patients.
Environmental measures at the waiting area and consultation rooms
Ventilation measurents were only available for 50 health facilities. Almost a half (22/50) of the facilities didn’t have adequate ventilated waiting areas based on the proportion of the window to floor area, Table
5. In addition, only 32% (17/50) of the facilities had the available windows fully open. In two facilities, there were louvered windows, with a wire mesh on the outside part of the windows, which prevented complete opening of the louvers, thus compromising ventilation. Structural improvements were reported in only three facilities and these facilities had a tent as waiting area. In most facilities, patients were observed to crowd in narrow and poorly ventilated corridors in outpatient departments, even where there was open area to wait from. Twenty four percent (12/51) of the facilities were not providing sputum diagnosis on site. For the facilities that were carrying out sputum diagnosis on site, 22/38 (58%) reported not having a designated area away from other patients and staff where patients can produce sputum specimens. Of those facilities which reported a designated area for sputum collection, 27% (4/16) reported this area being in the open air, 40% (6/16) near or behind the toilet, and 33% (6/16) anywhere in the facility.
Table 5
Ventilation assessment of out- and inpatient departments, consultation rooms, and laboratories in health facilities in Mukono and Wakiso
Outpatient Department | Adequate | 28 | 56 |
| Not adequate | 22 | 44 |
Consultation rooms | Adequate | 22 | 44 |
| Not adequate | 28 | 56 |
In-patient ward*
| Adequate | 17 | 37 |
| Not adequate | 29 | 63 |
Laboratory*
| Adequate | 17 | 37 |
| Not adequate | 29 | 63 |
Personal protective equipment
No facility had N95 respirators. In one facility, we observed sputum induction being carried on the ward with HCWs only wearing surgical masks to protect themselves.
Perceived barriers to implementation of TB infection control
Qualitative results
Structural barriers
A number of challenges were raised by HCWs. The most commonly cited barriers were; lack of space to implement the separation of TB suspects, both out and in-patient settings. Although the HCWs knew that TB suspects should be separated, it was reported that this was not possible due to lack of space in most facilities.
‘It is not possible here [patient separation] because we don’t have enough space. We don’t have a place where to put them [TB suspects].’ FGD Females
It was also reported in some FGDs that waiting rooms in facilities were small and poorly ventilated. All FGDs reported that, even minor structural changes were not possible. However, it was mentioned by three FGDs that because of the crowded and poor ventilated waiting areas, the TBCAP project gave them tents to be used as waiting areas. Unfortunately, in two facilities out of the three that were given tents, it was reported that the tents got torn. There was also a problem of not having chairs for the tents.
Lack of human resources
All FGDs reported that understaffing in their health facilities was a problem. TBIC measures like screening for people with cough, health education and timely sputum examination were seen as additional tasks for the already overstretched staff. It was reported that screening for cough as patients arrive was not done. In facilities where screening was done; it was reported to be carried out only in the consultation room and not as soon as they arrive at the facility.
‘Because sometimes you are busy doing other things you may not have time; you are busy giving injections. We are not so many; like now I am alone; I am the only enrolled nurse. If we were at least two, we would be doing the screening as they [patients] come… You just hear somebody coughing when you are here in the room, when you get out, you can’t even know who has been coughing. May be you ask and it may look embarrassing to a patient; they might say why are they asking me, is it bad to cough? So, it needs somebody who can sit there to just observe them.’ FGD Females
In one facility, it was reported that expert clients (HIV patients who work as volunteers) were used to give health education to patients in the waiting area, as a way to reduce the workload for the HCWs.
Stigma attached to TB
It was mentioned that there was reluctance of the staff to screen for patients with cough and separating them from other patients. Some FGDs reported that they were hesitant to tell a patient that they were suspecting TB and separating them from other patients when the TB diagnosis was not confirmed. Others felt that asking for cough at the reception (as the patient arrives) is part of history taking which should be done in the consultation room and not in public like in the waiting area. TB suspects were left seated with the other patients until it was their turn to go (‘first come first serve’) to the consultation room where screening for cough took place.
‘The problem is that we find it hard to tell them that, we are suspecting this [TB], you are not supposed to be with other people, sit alone. After all, the results might turn out to be negative.’ FGD men
Managerial support
Lack of funds to buy masks and to carry out renovations and structural improvements were also reported as challenges.
‘…But they didn’t carry it out; we put in our action plan to put some aeration to allow air flow through some of the corridors but it wasn’t done because of the funds.’ FGD Women
In one facility it was reported that the administration was not supportive enough, even when health workers made a request to shift the HIV clinic in their facility from a poorly ventilated place to an outdoor one.
“Like you see our TB/HIV premises, we are at a higher risk and when we were conducting the TB infection assessment, the ventilation was found to be at 0%. There is even darkness in the area and the worst thing is that these HIV patients are seated together with TB patients and some of them are suspects, and not yet on treatment. We requested to move the clinic to a more open, better ventilated place out there on the verandah, but it was rejected. So TB CAP came in and gave us a tent, which tent didn’t help us much because it came in without seats and immediately we put it up, it broke down and we didn’t use it. So we have remained in the same place up to today.” FGD Females.
Negative attitude towards TB among health care workers
Some FGDs reported that some HCWs have negative attitudes towards TB work. It was expressed that many HCWs were not interested in TB related work and therefore TBIC control is left to the staff working in the TB clinics. Some felt that there is no need to worry, since they have previously worked in the same environment without getting TB.
“Some clinicians don’t comply with separating TB suspects from other patients. They don’t appreciate why TB suspects should be triaged.” FGD male HCWs
“Am just wondering that recently they are making it a serious issue that health workers are at risk of acquiring TB from patients. We have worked here for years treating TB patients and none of us has ever got TB. Why the fuss now?” FGD Female HCWs
Two FGDs mentioned that support supervision and encouragement by district health officials to implement TB IC would motivate HCWs.
Lack of adherence among patients
The other challenges mentioned included patients being non-compliant with cough hygiene and not accepting to be separated. It was reported that where HCWs make an effort to implement the TBIC measures, patients don’t adhere to the instructions they are given.
Discussion
The findings in this study provide important information on the current status of implementation of TBIC measures in Uganda. Few health units had a TBIC plan and there was poor implementation of administrative measures like screening and separation of coughers. In addition, almost half of the facilities had poorly ventilated waiting areas. Reported barriers to implementation of TBIC included limited human resource, poor attitude towards TBIC by HCWs, lack of space and lack of funds.
Results from this study show that administrative control measures, the most important and most feasible measures in resource limited setting [
1] were not implemented. The situation was worsened by the inadequate ventilation (in waiting areas, consultation rooms and in-patient wards) and failure to open the windows. Reasons like lack of space and poor staffing levels accompanied with heavy workload, being given for the poor implementation of the administrative measures. Similar barriers have been reported in other settings [
32,
33]. This study has demonstrated a discrepancy between self-reported and observed TBIC practices. While 43% and 55% of the facilities were reported to screen and separate TB suspects, respectively, only 10% of them, were observed implementing both measures. This illustrates that HCWs relatively know what they are expected to do in terms of TBIC, but probably because of poor staffing levels and failure to appreciate the importance of TBIC, recommended measures are not implemented. This discrepancy between reported and observed measures also highlights the weakness of self-reports. Overestimation regarding compliance with guidelines due to socially desirable behavior in self-reports has been cited [
34].
The factors reported to hinder implementation of TBIC measures from the qualitative findings, emphasize the need for multi-pronged interventions in order to cause lasting behaviour change [
35]. In this study, such interventions would include solutions for human resource constraints, funding, supplies, structural changes in the facilities and managerial support. Thus for effective implementation of TBIC, the six health system building blocks-governance and leadership, health financing, access to supplies and human resource [
36] are in critical.
Most importantly, two FGDs mentioned that support supervision would motivate them to practice the TBIC measures. Providing feedback and the awareness of being observed has been reported to enhance hand hygiene [
35,
37]. This could be utilized in the implementation of TBIC too. Support from the administration in the staff efforts to implement TBIC is necessary for its successful implementation [
1]. Institutional administration support has been pointed as critical in general infection control [
37].
A qualitative study in Russia, [
38] found that fear of contracting TB was a motivator for implementing TBIC measures. In the current study HCWs seemed reluctant in implementing these measures, because they didn’t appreciate the importance of TBIC, after previously working in the same environment, without getting TB. An introduction of surveillance system for TB among HCWs is an important indicator of the quality of TBIC [
25]. This is critical considering the fact that Uganda has one of the highest TB default rate in the world of 10% [
25], high HIV prevalence of 7.3% [
27], the poor implementation of TBIC measures is a cause for concern.
This current study findings show that Mukono district was doing better than Wakiso, possibly due to the difference in the implementation approach. The TBCAP project provided additional support such as tents in some facilities, which was not the case in the MOH supported district. In addition whereas all facilities in Mukono had some people trained only selected facilities in Wakiso had people trained. Therefore, this difference might be due to more comprehensive support in addition to training, and the more inclusive training.
Our study had limitations. We only assessed the availability of IC measures and were unable to differentiate quality, comprehensiveness or consistency of implementation of all measures at assessed sites. For example a patient flow evaluation as an index of effective triage was not carried out. We also did not objectively measure the ventilation of the facilities using smoke tubes and anemometers. Thus we were did not get the actual air exchanges per second. However, the method we used gives an idea on the status of the ventilation. Non-differential misclassification with regard to presence or absence of different IC measures was reduced by use of interviews and observations. Though the tool that was used for the facility survey was not validated, it was pretested and the necessary adjustments made. The study was only carried out in two semi-urban districts in Uganda, which are close to the capital city, Kampala. However, the challenges affecting TBIC implementation i.e. health system challenges are generally the same across the country. Thus the practice and the challenges to implement TBIC in other areas may be even worse than the ones from the study districts. The qualitative findings from the FGDs, though not generalizable, together with the quantitative data provided a better understanding of the findings than either approach alone [
39].
Conclusions
Implementation of TBIC in Mukono and Wakiso districts in Uganda was poor. Limited resources such as lack of staff, funds and space and failure to appreciate the importance of TBIC precluded the adoption of even simple, cheap and most important TBIC interventions. Therefore, in ensuring implementation of the recommended TBIC practices, comprehensive support beyond training (e.g. human resources, providing masks, space and other alterations, support supervision, hands on support in development of TBIC plans and operationalizing them) are important.
Acknowledgements
We thank the study participants, research assistants, facility managers and the district health officials from both districts. We recognize the contribution of Dr. Vincent Batwala (Mbarara University of Science & Technology) and Dr. Juliet Kiguli and Dr. Simon Kasasa (Makerere University School of Public Health).
Funding
The funding was provided by KNCV TB Foundation, Netherlands, Belgium Technical Corporation (BTC), Belgium and the Carnegie Corporation, New York.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
EB, SV, BC, FN, RC, EMH, AK were involved in the development of the proposal. EB carried out field work. EB, FN, KJN, EMH, RW and RC undertook data analysis. EB, FN, KJN, EMH, SV, AK, RC, RW and BC drafted the manuscript and approved the final draft.