Our operational research showed that TB patients who were newly diagnosed as HIV-positive missed opportunities to be enrolled in HIV care. Firstly some TB patients who did not know their HIV status still missed the chance of testing although most patients had been successfully tested. Secondly many TB patients newly diagnosed as HIV-positive were not referred to ART clinic and not enrolled in HIV care properly. Lastly ART initiation and the ART regimen were also major issues even though these patients were enrolled in HIV care.
Once a patient is diagnosed with TB, HIV testing should be offered immediately if the HIV status is unknown. Other reports have already documented that integration of HIV and TB services improves the HIV testing rate among TB patients up to 94% in South Africa , 90% in Mozambique , 87% in Rwanda  and 91% in Malawi . Our study also showed the similar percentage of HIV testing among TB patients. In Zambia the scale-up of the policy for PITC and the decentralization of HIV care services through the national mobile ART services program could have contributed to such a high HIV testing rate for TB patients. However, around one tenth of TB patients still did not get tested despite that TB patients had higher risk of HIV co-infection in high burden country like Zambia. Further investigations are required to clarify the reason why they do not get tested.
The national guidelines for ART and TB recommend that active TB patients co-infected with HIV should be promptly and effectively referred to HIV care [9, 10]. However, referrals from TB to ART clinics were still inadequate in the primary healthcare setting. Furthermore, various factors such as male sex, history of previous TB treatment, registration site, registration year, and death on TB treatment outcome were identified as strongly associated with enrolment in HIV care. The guidelines also recommend that TB/HIV patients should commence ART according to CD4 cell count and patient condition, and that an efavirenz-based regimen is preferred to a NVP-based regimen. Although we found that most of the patients initiated ART during TB treatment, NVP-based regimen was still widely used for patients on TB treatment.
Operational implementation of TB/HIV integrated healthcare remains a major challenge in primary healthcare despite the availability of national guidelines for optimal TB/HIV co-treatments. Our analysis suggested that issues involving healthcare workers, the health services system, and patients were all implicated in the substandard treatment of many TB/HIV patients which resulted in the poor linkage between TB and HIV services.
In some resource-limited settings, TB and ART clinics still function independently at the operational primary healthcare level [11, 12], although some pilot projects have successfully integrated TB and HIV services [6, 13–16]. There are three steps in operational settings for proper care of TB/HIV patients: 1) referral from the TB clinic; 2) attendance at an ART clinic and enrolment in HIV care; and 3) commencement of ART. Our results revealed that only 59.3% of TB/HIV co-infected patients (176/297) were referred from a TB clinic to an ART clinic, and 34.1% (85/297) were enrolled in HIV care, with only 16.2% (48/297) commencing ART during TB treatment. This suggests that healthcare workers at TB clinics might have been satisfied with only screening for HIV, thereby neglecting the referral of co-infected patients to ART clinics.
Pre-treatment loss to follow-up has been strongly associated with poor quality health services and minimal commitment on the part of healthcare workers [17, 18]. The healthcare workers at the TB clinics may have mismanaged of providing options available for co-infected patients despite that all workers have already trained for TB/HIV care services. For example, a lack of sufficient information regarding the patients’ condition may have affected the results, such that patients may have chosen not to visit ART clinics and be enrolled in HIV care due to their lack of understanding of the disease and its treatment. Those patients who were not referred from a TB clinic showed a significantly lower enrolment rate in HIV care. The failure of all TB/HIV co-infected patients to be enrolled in HIV care may arise from poor service from healthcare workers, and would also affect the outcomes of these patients. Recent clinical trials have shown that earlier initiation of ART during TB treatment in patients co-infected with HIV significantly reduced mortality compared with patients initiating ART after TB treatment completion [19–22]. Death on TB treatment outcome was also associated with the enrolment in HIV care. The median days between the date of TB treatment initiation and the date of death in non-enrolled group was significantly shorter than that in enrolled group (31.0 vs. 86.5 days; p < 0.01) (not shown on the table). Some patients may have died before enrolment in HIV care. Patient’ earlier access to health facilities and earlier diagnosis and treatment might need to be more advocated among people in communities by health care workers to avoid these bad outcomes.
The linkage of patient information between TB and ART clinics also requires to be coordinated more effectively by healthcare workers at both clinics. Since TB and HIV registers and records were maintained separately at their respective clinics, and no information was exchanged directly, a lack of coordination may have influenced the low percentage of co-infected patients being enrolled in HIV care and receiving optimal treatment. In our study, the patients who were treated with the NVP-based regimen had a significantly higher percentage of their HIV case records missing TB treatment information. When healthcare workers at an ART clinic do not realize that the patient is receiving TB treatment, the NVP-based ART regimen may be given. This regimen has been shown to increase virological failure and mortality because of drug interactions between rifampicin (used to treat TB) and NVP . Thus, sharing information between the two clinics would improve patients’ outcomes through healthcare workers providing appropriate monitoring and continuity of care to the patients.
Health services system
Of the patients registered at RHCs, a significantly higher number of patients were enrolled in HIV care at the RHCs where ART services were available, although a small number of newly diagnosed HIV patients were enrolled in HIV care at non-ART sites.
Difficulties in transferring patients from a non-ART site to an ART site could explain the significantly lower enrolment at non-ART sites. It concurs with other studies which reported that the availability of one-stop services for TB and HIV at the same facility promoted the linkage between these two services [6, 16, 24]. In Zambia, decentralization of ART services through the national Mobile ART Services program, allowing HIV care delivery in areas without the services, was adopted as the national policy for one-stop services to strengthen linkage. However, even at ART sites, only 30.4% of the patients (84/276) were enrolled in HIV care. The clinic schedules, in which the TB clinic opens daily but the ART clinic opens every 2 weeks when the mobile ART services come, might also affect the enrolment of patients. Management of a patient’s appointments on the same day by both clinics requires strengthening to offer a one-stop service in terms of place and time.
Compared with patients registering at the TB clinics in 2009, there were twice as many patients registered in 2010 who were enrolled in HIV care. The activities of the TB/HIV coordinating committee organized by Chongwe District Medical Office at the end of 2009, likely contributed to this marked improvement. This committee has launched awareness campaigns for both healthcare workers and patients, and introduced a patient escort service to facilitate appropriate referrals between the two clinics at some RHCs. Not only national policy, but also local policy reflecting the operational situation, could play important roles in improve linkage of services especially in primary healthcare.
Male sex and previous TB treatment were negatively correlated with enrolment in HIV care. No other studies have reported an association between these factors and enrolment in HIV care, though a number of studies have shown that male sex is associated with problems complying with ART. One study in South Africa reported an association between male sex with non-initiation of ART during TB treatment . Others reported that men had higher early mortality on ART due to their presentation at a more advanced stage of disease [26, 27], and a higher risk of ART treatment default . These studies imply that males may have more apathy, a lack of insight and lower acceptance of not only ART but also HIV care. For example, in the real settings, men’s working schedule might have influenced their lower enrolment in HIV care. Working for their family would be more prioritized for them than going to the clinic.
We also found that patients with previous TB treatment were less likely to be enrolled in HIV care. Since some studies have reported that previous TB treatment is a risk factor for subsequent TB treatment default [29, 30], it could also be a factor for defaulting in enrolment in HIV care. It might be related to attitudes among some group of cases called “defaulter personality”. Personal and/or social factors, such as financial burden and lack of social support, are important determinants of treatment adherence . It might also affect the enrolment in HIV care among TB/ HIV co-infected patients. The previously treated TB patients also have to present to the TB clinic every day for streptomycin injections. A prolonged and more complex treatment with daily intramuscular injections coupled with more side effects and might increase the risk of quitting TB treatment and rejecting being enrolled in HIV care. However, the national guidelines for TB recommend that re-treatment must be administered under strict directly observed treatment during the entire therapeutic process . These patients should have more opportunity to be enrolled in HIV care since they visit the health facility more often and are closely observed by healthcare workers. Failure in the enrolment in HIV care may also result from a lack of action by healthcare workers as already discussed above. Although the shortage of healthcare workers might affect the situation especially at the primary healthcare level, the proper referral protocol based on the national guidelines also requires to be reinforced through the re-fresher trainings.
This study has several limitations. First, there was a relatively small number included in the study. As decentralization of ART services through the national Mobile ART Services program were set up properly at selected RHCs in the middle of 2008, only information for 2009 and 2010 was available to evaluate the linkage between TB and HIV services at the primary healthcare level.
Patient information was obtained through routinely collected data in RHC registers. Matching of TB/HIV co-infected patients at ART clinic was done using the electronic information system for HIV patients. Although we tried to minimize missing or inaccurate data by asking all RHC staff to record and input patient data properly, some information bias in the data could be present. We may also have underestimated the number of enrolled patients, since our confirmation of enrolment in HIV care was done at ART clinics only within the district. However, maximum efforts to trace patients were made by RHC staff and community volunteers, which reflected the operational situation.
Although the sites for the mobile ART program rollout were selected randomly by the district medical office to cover as large an area as possible, ART sites had a greater burden of TB cases per site than non-ART sites. This could suggest the presence of a selection bias which might have affected our results. However there was no statistically significant difference between sites in the HIV testing rate (88.0% in ART sites, 91.3% in non-ART sites; p = 0.43) and the prevalence of newly diagnosed HIV (82.9% in ART sites, 77.7% in non-ART sites; p = 0.44).