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Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review a
Karolina Griffiths & Nathan Ford a
b
Liverpool School of Tropical Medicine , Liverpool , UK
b
Centre for Infectious Disease Epidemiology and Research , University of Cape Town , South Africa Published online: 22 Aug 2013.
To cite this article: Karolina Griffiths & Nathan Ford (2013) Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review, Medicine, Conflict and Survival, 29:3, 198-215, DOI: 10.1080/13623699.2013.813108 To link to this article: http://dx.doi.org/10.1080/13623699.2013.813108
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Medicine, Conflict and Survival, 2013 Vol. 29, No. 3, 198–215, http://dx.doi.org/10.1080/13623699.2013.813108
Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review Karolina Griffithsa* and Nathan Fordb
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a
Liverpool School of Tropical Medicine, Liverpool, UK; bCentre for Infectious Disease Epidemiology and Research, University of Cape Town, South Africa (Accepted 5 June 2013) Providing antiretroviral treatment (ART) in humanitarian settings is challenging. Reports suggest that ART provision is feasible, but the evidence base is scarce. We systematically searched three databases for studies reporting ART outcomes among displaced populations in settings of conflict, natural disasters or political instability, and estimated overall mortality using random effects models. Fourteen studies were identified, six in conflict areas, five in areas of post-election violence and three in natural disaster settings. The pooled proportion for mortality was 7.6% (95%CI 5.3–10.0%) at six months and 9.0% (95%CI 5.8–12.2%) at 12 months. Loss-to-follow-up at six months was 6.3% (95%CI 4.3–8.3%) and at 12 months was 8.1% (4.9–11.2%). Adherence was comparable to stable settings. Strategies used to support ART provision included additional drug stocks and establishing peer communication networks. Good clinical outcomes can be achieved with ART in disaster setting, in particular if supported by regional collaboration, standardized drug regimens and contingency planning. Keywords: antiretroviral; displaced; humanitarian; HIV; disaster; conflict
Introduction Displaced populations face numerous challenges in accessing antiretroviral therapy (ART), including individual challenges such as transport and loss of income, health service challenges such as disruption to services and drug supplies, and social challenges such as stigma and lack of social support. These challenges, together with the existence of competing health priorities such as malnutrition and tuberculosis, have raised concerns about poor adherence to ART in conflict settings (UNHCR and Southern African HIV Clinicians Society 2007; Olupot-Olupot et al. 2008). Good adherence to ART is essential to ensure optimal health outcomes and limit the development of drug resistance (Esté and Cihlar 2010). *Corresponding author. Email: karolinagriffi[email protected] Ó 2013 Taylor & Francis
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Because of these concerns, international guidance has until recently been hesitant about promoting access to ART in humanitarian emergencies (Ellman, Culbert, and Torres-Feced 2005; The Sphere Project 2011). However, emerging evidence suggests that ART provision is feasible in conflict and disaster humanitarian settings (Kiboneka et al. 2009; O’Brien et al. 2010), and more recent guidelines published by UNHCR and SPHERE have acknowledged the need to provide ART to displaced populations (UNHCR and Southern African HIV Clinicians Society 2007; The Sphere Project 2011). This systematic review summarizes the evidence regarding the effectiveness of ART care in conflict and disaster settings and identifies strategies to support ART adherence in these unstable settings. Methods A systematic literature search was undertaken in PubMed and EMBASE from inception to 1 April 2013 combining key search terms (see Appendix). We additionally screened abstracts of all conferences of the International AIDS Society up to July 2012. Published articles were screened by title and abstract by one author (KG) and agreement on final inclusions was made in duplicate (KG, NF). Searches were limited to English language publications. The bibliographies of full text articles were searched for potentially relevant articles. Studies were selected according to pre-defined inclusion criteria which sought original research articles reporting ART outcomes among HIV positive adults and children who had been displaced due to a humanitarian crisis (defined as conflict, natural disaster or political instability). The primary outcome was mortality and secondary outcomes included virological suppression, CD4 gain, development of drug resistance, adherence (as defined by the studies) loss to follow up, and missed appointments (as defined by the studies). We assessed study quality based on study design, selection or measurement bias, standard case definitions used, follow up of patients, whether confounders were controlled/adjusted and if confidence intervals were provided; this assessment was based on guidelines from the National Institute for Health and Clinical Excellence in the United Kingdom (National Institute for Health and Clinical Excellence 2012), which has been used by other systematic reviews of health challenges in conflict (Kimbrough et al. 2012). No study was excluded on the basis of poor methodological quality. For the primary outcomes of mortality and lost to follow-up we calculated point estimates and 95% confidence intervals for the proportion of patients who had died at different time points. Proportions were stabilized through arcsine square-root transformation and pooled using a DerSimonian–Laird random effects model. All analyses were done in Stata version 12.0.
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Results Characteristics of included studies After screening 6457 titles, fourteen studies were included in this review (Figure 1). Six studies were carried out in armed conflict settings (Kiboneka et al. 2008; Garang, Odoi, and Kalyango 2009; Kiboneka et al. 2009; O’Brien et al. 2010; Salami, Buzu, and Nzeme 2010; Autino et al. 2012). Two studies (Culbert et al. 2007, Vreeman et al. 2009) reported results that were reported by other included studies (O’Brien et al. 2010; Yoder et al. 2012) and were excluded from the final review. Five studies reported outcomes in a setting of post-election violence (Unge et al. 2010; Pyne-Mercier et al. 2011; Bamrah et al. 2013; Doumbouya et al. 2012; Yoder et al. 2012); these studies were undertaken mainly in sub Saharan African, where both HIV and conflicts are most prevalent (Mills et al. 2009), including Kenya, Northern Uganda and the Ivory Coast. Three studies reported outcomes from natural disaster settings (Bhakeecheep et al. 2012; PUBMED 3527 titles & abstracts screened
EMBASE 1735 titles & abstracts screened
IAS Abstracts screened 1195
All References screened
Read in full: 22
Read in full: 13
Read in full: 61
Read in full: 3
Excluded: - 59 (not relevant)
Excluded: - 1 (Culbert 2007) as data reported by another study
Included: 2
Included: 2
13 Excluded as did not fit inclusion criteria: - 3 studies not in crises situation - 2 studies not on ART - 1 study looked at access not provision - 2 discussed organisational issues - 2 case studies not original research - Yoder et al. data replicates Vreeman et al -1 study had qualitative data only - 1 study, no denominator of data
Excluded: - 2 duplicates Seven did not fulfil inclusion criteria: - 2 studies no data on ART - 1 study not original research article - 1 study, no recent data post disaster - 3 studies included migrant workers not in crises situation
Included: 9
Included: 4
3 duplicates
Final Number of articles for inclusion: 14
Figure 1.
Search Strategy.
Snapshot.4 days for adherence.
3 months (22/09/1121/12/11)
Post-election violence
Flooding crisis
Post-election crisis
Armed Conflict
Flooding crisis
Bamrah et al. 2013
Bhakeecheep et al. 2012
Doumbouya et al. 2012
Garang, Odoi, and Kalyango 2009
Khawcharoenporn et al. 2013
Jan-June 2011
6 months. JulyDecember 2011
Survey. One interview day, 10 weeks after election
4 years, 7 months (01/01/ 07- 15/08/11)
Political crisis/ migrant workers from conflict
Autino et al. 2012
Reporting period
Type of crisis
Summary table of study characteristics.
Author
Table 1
Rural district, in CentralWest Burkina Faso 3 provinces in Kenya, Rift Valley, Nyanza, Central 22 provinces in Lower North and Central Thailand 5 health regions in conflict in Ivory Coast Urban, IDP camp and surrounding area, Gulu, Northern Uganda Central Thailand
Study setting
1.20% (UNAIDS)
6.5 % (UNAIDS 2009)
3% (UNAIDS, Adults)
1.20% (UNAIDS)
6.7% (national)
1.3% in rural district of Burkina Faso
Estimated regional/national HIV prevalence at time of study
HIV clinic at large referral hospital
Lacor Hospital,
68 healthcare centres
35 health facilities providing ART and 9 IDP camps 242 Hospitals
Nanoro District Hospital
Place of care Age (years)
Unclear
Missionary not- for – profit organisation
NGOAconda
Government
40
Unclear
NR
NR
Government 40 and European ESTHER alliance Not clear 37 years, 39.1 in IDP camps
Provider
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(Continued)
45% (97/217)
67.5 % (135/200)
NR
NR
70%, 64% in IDP camps
40.3% (56/139)
Female (%)
Medicine, Conflict and Survival 201
12 months
Armed conflict or post conflict settings
Post election violence
O’Brien et al. 20101
Pyne-Mercier et al. 2011
Armed conflict
Snapshot, Feb 2008.
Armed Conflict
Kiboneka et al. 2008
2 months. 30/12/2007 -28/02/2008
2 years, 7 months (8 June 2005 – 29 Jan 2008)
Armed conflict
Kiboneka et al. 2009
Reporting period
Type of crisis
Author
Table 1. (Continued).
Western equatorial
Urban IDP camp and surrounding area, Gulu Northern Uganda Urban IDP camp and surrounding area, Gulu Northern Uganda. 12 programmes11 Sub Saharan Africa, 1 India. Most rural. 2 refugee camps. Nairobi
Study setting
12.1% (regional)
7.8%
1- 10 %
6.5% (UNAIDS 2009)
6.5% (UNAIDS 2009)
Estimated regional/national HIV prevalence at time of study
HIV clinic
One HIV clinic
Clinics and hospitals.
District hospital.
Lacor Hospital,
Place of care
Faith based Not-for-profit organisation, funded by PEPFAR International organisations,
NGO (MSF)
Missionary not for profit organisation.
Missionary not- for – profit organisation
Provider
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NR
37
35
8
39
Age (years)
NR
(Continued)
63.8% (1617/ 2534)
66%
60% (34/57)
72% 1162/1625
Female (%)
202 K. Griffiths and N. Ford
Postelection violence
Yoder et al. 2012
14 months (26/10/200731/12/2008)
5 months post earthquake (12 January May 2010)
9 months. July 2009-March 2010 1 month (01.01.200801.02.2008)
Urban and rural, Western Kenya
state Southern Sudan Informal urban settlement, Kibera, Nairobi, Kenya Rural and urban, Haiti
Study setting
7.8% (Adults and children)
1.9%
7.8%
African Medical Research Foundation
supported by WHO
Provider
50 PEPFAR Ministry of supported public health, sites international and national NGOs. One urban AMPATH2 referral hospital,26 urban and rural clinics, 23 satellite clinics
One HIV Clinic
Place of care
NR
50.2% (1269 of 2549 children on or off ART)
Unclear for those on ART
NR
Female (%)
NR
NR
Age (years)
Notes: 1O Brien et al includes data from separate studies.2AMPATH – USAID-Academic Model Providing Access to Healthcare clinical care system, a joint initiative between Indiana University School of Medicine, Moi University School of Medicine, Kenya and Moi Teaching and Referral Hospital.
Post-earthquake
Postelection violence
Salami, Buzu, and Nzeme 2010 Unge et al. 2010
Reporting period
Estimated regional/national HIV prevalence at time of study
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Walldorf et al. 2012
Type of crisis
Author
Table 1. (Continued).
Medicine, Conflict and Survival 203
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Walldorf et al. 2012; Khawcharoenporn et al. 2013). Finally, two studies only reported results for children (Kiboneka et al. 2008; Yoder et al. 2012). Four studies were supported by non-governmental organizations and four sites were run by faith-based organizations (Table 1). All programmes provided ART free of charge. The average age of adults in the studies ranged from 35–40 years and for children was 8 years. Of the studies that reported sex of participants, the majority (7/9) included more women than men. Baseline CD4 counts ranged from 97–224 cells/mm3.
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Assessment of study quality All of the included studies were observational cohorts. Three of the studies were published as abstracts, and did not provide enough information to fully assess the study methodology (Salami, Buzu, and Nzeme 2010; Doumbouya et al. 2012; Bhakeecheep et al. 2012). Nine of the studies did not statistically adjust for confounders and seven studies did not follow up patients for more than six months. Two studies were given a ‘higher rating’ of overall strength of study quality (Kiboneka et al. 2009; Yoder et al. 2012), five studies were given a ‘medium’ rating, (Garang, Odoi, and Kalyango 2009; O’Brien et al. 2010; Autino et al. 2012; Walldorf et al. 2012; Khawcharoenporn et al. 2013) and seven studies a ‘lower’ rating (Kiboneka et al. 2008; Salami, Buzu, and Nzeme 2010; Unge et al. 2010; Pyne-Mercier et al. 2011; Bamrah et al. 2013; Bhakeecheep et al. 2012). (See Supplementary Table 1 available on the publisher’s website at http://dx.doi.org/10.1080/13623699.2013.813108) ART outcomes Three studies reported mortality data from 14 cohorts across seven countries. Mortality at six months ranged from 1.0% (95%CI 0.9–8.2%) to 28.3% (95% CI 11.7–37.1%) with a pooled proportion of 7.6% of patients having died (95%CI 5.3–10.0%). Mortality at 12 months ranged from 2.6% (95%CI 2.2–20.6%) to 28.0% (95%CI 9.5–51.8%) with a pooled proportion of 9.0% of patients having died (95%CI 5.8–12.2%). (Figure 2.) Loss to follow up was reported by three studies (14 cohorts) and the pooled proportion was 6.3% (95%CI 4.3–8.3%) at six months and 8.1% (4.9–11.2%) at 12 months. CD4 gain was reported by two studies (Table 1). Changes in six month CD4 counts ranged from 129–187 cells/mm3. Adherence, reported by six studies, was over 80% in all settings, with four studies reporting adherence rates of over 90%, (Kiboneka et al. 2008; Garang, Odoi, and Kalyango 2009; Kiboneka et al. 2009; Yoder et al. 2012). Missed appointments were reported in seven studies using different definitions over varying time periods (Table 1). In settings of political crisis, 4.7–11% of patients missed appointments in Kenya and 16.1% described
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Setting
Proportion (95% CI) n
Duration
205
e
6 months 6 months CAR Bogulia Cote d'Ivoire, Danane 6 months 6 months DRC, Dubie 6 months DRC, Kilwa 6 months DRC, Baraka 6 months DRC, Bukavu 6 months DRC, Walikale 6 months India, Manipur 6 months RoC, Kindamba 6 months RoC, Kinkala 6 months RoC, Mindoull 6 months Uganda Kitkum Subtotal
6.60 (1.97, 13.66) 6.13 (4.17, 8.45) 28.32 (13.91, 45.47) 23.16 (11.70, 37.12) 15.53 (8.24, 24.61) 8.00 (6.66, 9.45) 0.97 (0.87, 8.23) 4.09 (2.79, 5.63) 19.37 (4.97, 40.19) 16.64 (6.10, 31.02) 6.02 (3.10, 9.82) 8.22 (3.22, 15.24) 7.62 (5.29, 9.96)
67 480 29 40 73 1443 25 745 17 32 190 78
4 29 8 9 11 115 0 30 3 5 11 6
12 months 12 months CAR Bogulia Cote d'Ivoire, Danane 12 months 12 months DRC, Dubie 12 months DRC, Kilwa 12 months DRC, Baraka 12 months DRC, Bukavu 12 months DRC, Walikale 12 months India, Manipur 12 months RoC, Kindamba 12 months RoC, Kinkala 12 months RoC, Mindoull 12 months Uganda Kitkum Subtotal
6.19 (0.93, 15.63) 8.99 (6.14, 12.32) 28.07 (9.50, 51.80) 27.13 (13.91, 42.84) 18.26 (9.05, 29.80) 11.05 (9.39, 12.81) 1.82 (1.60, 14.96) 4.14 (2.74, 5.82) 2.57 (2.20, 20.57) 6.70 (5.12, 46.64) 8.40 (4.20, 13.87) 14.96 (4.69, 29.67) 9.00 (5.75, 12.24)
39 327 15 34 51 1289 13 639 9 3 124 29
2 29 4 9 9 142 0 26 0 0 10 4
NOTE: Weights are from random effects analysis -51.8
0
51.8 Percentage
Figure 2.
Pooled proportion for mortality.
treatment interruptions. Service delivery was a concern with almost a half of centres in the Ivory Coast failing to deliver ART. No studies reported virological suppression as an outcome. No studies reported development to drug resistance, although one abstract highlighted the need to monitor drug resistance throughout ART programmes (Bhakeecheep et al. 2012). Within natural disaster settings patient retention was high. During floods in Thailand 10% (4167/41,673) of patients had missed one appointment or more (Bhakeecheep et al. 2012). Only 7/217 HIV patients on ART at one HIV clinic in Thailand reported no access to treatment during the disaster (Khawcharoenporn et al. 2013). Walldorf et al. (2012) reported that 97% of current patients on ART from the baseline pre-earthquake were followed up in the following four months post-earthquake. This was reduced to 90.5% in areas that were affected most by the earthquake; however the ART programme continued to enrol patients five months post earthquake.
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Strategies to support ART delivery A range of strategies were reported by the studies to support ART delivery, including regional collaboration between other HIV care services, patient education and adherence counselling, standardized drug regimens/treatment protocols, establishing a communication network between patients, and provision of additional medication stock to patients in case of crisis (Table 2). One study reported that decentralization of ART services may improve access (Pyne-Mercier et al. 2011). Another study (Autino et al. 2012) established a formal international transfer process between sites in Burkina Faso and the DRC, an example of effective continuity of care. Patient follow up within humanitarian settings is complicated by disrupted transport facilities and security concerns. Proposed solutions reported by the studies in this review included extending peer networks, using computerized record keeping to highlight when drug refills are necessary (Unge et al. 2010), peer ART delivery (Bhakeecheep et al. 2012), and mobile telephones to aid with follow up of patients (Autino et al. 2012; Bamrah et al. 2013; Walldorf et al. 2012) and sending adherence reminders (Bhakeecheep et al. 2012). In Thailand, reducing restrictions on second line regimens was recommended (Bhakeecheep et al. 2012). Other authors recommended ensuring drug regimens are standardized across the region in case of population displacement (O’Brien et al. 2010). The importance of disaster preparedness and collaborative activities between patients, healthcare providers and government was highlighted, with Khawcharoenporn et al. (2013) separating strategies into preflood, flood and post-flood period. Discussion The effectiveness of ART is well established, and the extent to which good treatment outcomes can be achieved in disaster settings depends on a range of delivery challenges including continuity of drug supply, innovative approaches to supporting patient adherence, and access to services for patients and health staff to dispense drugs. Our review found that overall ART outcomes were satisfactory. Mortality, loss-to-follow-up, and adherence were all within the range reported by ART programmes in stable programmes in resource-limited settings (Braitstein et al. 2006; Mills et al. 2006; Rosen, Fox, and Gill 2007). These findings are consistent with those reported by a recent review of antiretroviral adherence in conflict-affected and forcibly displaced populations which reported satisfactory levels of adherence compared to non-affected groups (Mendelsohn et al. 2012). Only 14 studies were eligible for inclusion in this review, despite using a broad search criteria that resulted in an extensive search of both published literature and conference abstracts. This limitation in the evidence base may be due to the difficulties and challenges of undertaking research in conflict and
139 migrant workers returning from Demoncratic Republic of Congo (134), Ghana (3) and France (2). 107 on ART
1’294 facility based respondents, 336 IDPs
41’673 PLWHA receiving ART in 242 hospitals 17’471 PLWHA receiving ART in 68 centres 200 Adults (>18)
Autino et al. 2012
Bamrah et al. 2013
Bhakeecheep et al. 2012
Garang, Odoi, and Kalyango 2009
Doumbouya et al. 2012
Participants
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
Missed appointments (varied methods of reporting)
NR
NR
NR
NR
(Continued)
4167/ 41,673 (10%) had 1 missed appointment or more 32/68 (47%) centres failed to deliver ART
4.7% (rift valley), 6.8% (Nyanza), 11% (Central province) not returned to routine health care facilitiy since post election unrest
14/107 (13.1%) NR over 43 months.10.2 per 100 patients per year
Loss to follow up (varied time periods recorded)
NR 99.6% Adherence amongst IDPS (>95% adherence levels over 4 days, self reports) compared to 99.5% Non IDPs
NR
During Jan 2008:31 (17.6%) in Rift Valley, 24 (9.3%) in Nyanza, 9 (4.8%) in Central province of patients reported missing therapy.83.6 (Rift Valley), 42.9 (Nyanza), 28.9 (Central) therapy days missed per 1000 NR
NR
NR
Virological CD4 cell suppression count Baseline: 224 (+/– 184)After 6 months: 411 (+/– 305)Mean gain of 187 cells/mm3 NR
Drug resistance development Adherence
NR
16/107 (15%) over 4 years, 7 months. 11.6 per 100 patients per year
Mortality
Summary table of study outcomes.
Author
Table 2.
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Participants
217 adults
1625 Adults
57 Children
4145 adults2572 with 12 month data
2534 adult patients
159 adults
722 patients
Author
Khawcharoenporn et al. 2013
Kiboneka et al. 2009
Kiboneka et al. 2008
O’Brien et al. 2010
Pyne-mercier et al. 2011
Salami, Buzu, and Nzeme 2010
Unge et al. 2008
Table 2. (Continued).
NR
NR
NR
9% Mortality of those on ART, 12 months.
Mortality rate: 69/ 1625 (4.2%) from 08/06/2005 to 29/ 01/2008Mortality Incidence Rate: 3.48 (95% CI 2.66 to 4.31) per100 person years NR
NR
Mortality
NR
NR
NR
Mean baseline: 97 cells/ mm3
Median baseline: 139 cells/ mm3Median gain at 6 months: 129 cells/ mm3 NR
NR
NR
NR
Baseline: median 144 cells/mm3 Baseline median: 157 (90–220)
NR
NR
NR
Virological CD4 cell suppression count
NR
NR
NR
NR
90/102 (88%) reported adherence levels > 95% (missed less than 3 doses in past month) NR
NR
92.2% had good adherence (>95% combination ART adherence, measured by pharmacy monitored drug possession ratio, pharmacy refill records and 3 day recall report) 92% had good adherence (>95% adherence) NR
NR
NR
NR(only pre flood data)
NR
Drug resistance development Adherence
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NR
NR
NR
466/2572 (11%)
(Continued)
186 of 447 (42%) of scheduled appointments were missed
408/2534 (16.1%) experienced treatment interruptions NR
NR
NR
NR
NR
7/217 (3%) self reported no access to ART during study period NR
Missed appointments (varied methods of reporting)
NR
Loss to follow up (varied time periods recorded)
208 K. Griffiths and N. Ford
24,863 patients on ART baseline December 2009.
1627 children under the age of 14 on ART
Walldorf et al. 2012
Yoder et al. 2012
Note: NR = not reported.
Participants
Author
Table 2. (Continued).
NR
NR
NR
NR
Mortality
NR
NR
Virological CD4 cell suppression count
NR
NR
91.8% (1’494/1627) had perfect adherence (defined as taken “all” pills in past 7 days) 4 months post election and 91% (1481/1627) had perfect adherence 5-10 months post election
NR
Drug resistance development Adherence
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3% (49/1627) initial loss to follow up, 2.6% (42/1627) after 12 months
NR
Loss to follow up (varied time periods recorded) 3% fewer patients attended clinical examination visit for ART 3 months post earthquake. 3.9% increase from baseline 4 months post earthquake. NR
Missed appointments (varied methods of reporting)
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disaster settings. Only three studies reported outcomes of ART delivery in natural disasters, despite the evident need to continue to address ART provision in these difficult circumstances. For example, a study from Tete province in Mozambique during prolonged drought highlighted the need to align food aid and HIV programmes (Renzaho 2007); however, this study did not report outcomes that could allow for its inclusion in this review. Several recommendations to improve ART in displaced populations in humanitarian settings emerge from this review. Key issues include contingency planning and coordination between organizations to ensure continuity of care. It is necessary to bridge ART between emergency aid in relief situations and in the development phase to ensure long-term use. Improved collaboration between non-governmental organizations (NGO) and the private services may allow patients to access ART from a greater range of health facilities (Unge et al. 2010). Patients were reported to receive ART and care from other provider sites, but may not have medical notes detailing these visits (Vreeman et al. 2009). Healthcare providers should keep up-to-date lists to inform patients of alternate regional clinic sites and pharmacies during an emergency (Walldorf et al. 2012). Contingency planning has been shown to be effective in improving adherence (Culbert et al. 2007). Despite the risk of medications being lost or sold, it is necessary to consider providing medication for extended periods when violence or political instability is predicted (Unge et al. 2010). Busy periods may be predicted, for example post-election periods or where rising tensions are documented between groups known to be associated with violence and conflict, and ART providers should recognize this and ensure contingencies are put in place (Pyne-Mercier et al. 2011). Certain ‘at-risk populations’ may have increased difficulties during a crisis, it is vital to understand the political ethnic compositions of a region in order to optimize care (Yoder et al. 2012). Some study sites reduced non-essential services to a minimum in order to prioritize and successfully continue ART provision (O’Brien et al. 2010; Doumbouya et al. 2012). This review has several limitations to note. The database search was only run in English, and studies published in other languages may exist. Publication bias may be a concern, as organizations may be less willing to report negative outcomes, and risk of bias is a concern given that all studies were observational and the majority were rated as medium or low quality. Many of the studies were from well-supported sites that received external support from international agencies, and outcomes may be different in contexts where such additional support is lacking. Finally, most studies in this review came from conflict settings in sub-Saharan Africa, and challenges and solutions may be different in other contexts. Organizations involved in the provision of ART in humanitarian settings are encouraged to report their approaches and outcomes, particularly in response to natural disasters, as these are under-represented in the literature.
X X
X
X
X X
X
X
X
X
X X
Additional drug stocks for patients
X
X
Standardize drug regimens/ treatment protocols
X
X X
Good collaboration with regional health services/ NGOs
X
X
Duplicate medical records
X X
X
X X
X
X
X
X
X
X
Patient education and adherence counselling
X
X
X
X
X
Electronic Medical Follow up Record outreach System programme
Strategies recommended to improve care in displaced populations in humanitarian settings.
Autino et al. 2012 Bamrah et al. 2013 Bhakeecheep et al. 2012 Doumbouya et al. 2012 Khawcharoenporn et al. 2013 Kiboneka et al. 2009 O’Brien et al. 2010 Pyne-Mercier et al. 2011 Salami, Buzu, and Nzeme 2010 Unge et al. 2010 Vreeman et al. 2009 Walldorf et al. 2012
Table 3.
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X
X
X
X
X
X X
X
X
X
X
Communication Networks with Task Operational Patients Shifting research
Medicine, Conflict and Survival 211
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In conclusion, despite a clear recognition of the need to ensure continuity of care for people living with HIV affected by humanitarian disaster there remains a lack of reporting on approaches to improve the effectiveness of ART in humanitarian settings. Nevertheless, outcomes are generally encouraging, and demonstrate that with approaches such as improved collaboration, standardized drug regimens and improved preparedness it is possible to achieve the same outcomes in humanitarian settings as in stable settings. Acknowledgements
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The authors would like to acknowledge Timothy O’Dempsey for his advice and support.
Supplemental data Supplemental data for this article can be accessed here: http://dx.doi.org/ 10.1080/13623699.2013.813108 Notes on contributors Karolina Griffiths is a Royal Liverpool University Hospital foundation doctor, a graduate of the University of Liverpool and the Liverpool School of Tropical Medicine. Nathan Ford is a research associate at the University of Cape Town with a special interest in the delivery of antiretroviral therapy in resource-limited settings.
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Doumbouya, B., M. Zaho, S. Adouko, E. Komena, B. Mensah-Maika, and S. Touré. 2012. “The Challenge of Maintaining Continuum of Care and Support to PLHIV in Health Facilities Located in Military Conflict Zones in Ivory Coast. Abstract.” 19th International AIDS Conference. Abstract no. THPDE0203. Ellman, Tom, Heather Culbert, and Victorio Torres-Feced. 2005. “Treatment of AIDS in Conflict-affected Settings: A Failure of Imagination.” The Lancet 365 (9456) (01/ 22): 278–280. Esté, José, A., and Tomas Cihlar. 2010. “Current Status and Challenges of Antiretroviral Research and Therapy.” Antiviral Research 85 (1) (01): 25–33. Garang, P. G., R. A. Odoi, and J. N. Kalyango. 2009. “Adherence to Antiretroviral Therapy in Conflict Areas: A Study Among Patients Receiving Treatment from Lacor Hospital, Uganda.” AIDS Patient Care & Stds 23 (9) (Sep): 743–747. Khawcharoenporn, Thana, Anucha Apisarnthanarak, Krongtip Chunloy and Linda M. Mundy. 2013. “Access to Antiretroviral Therapy During Excess Black-water Flooding in Central Thailand.” AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV. http://dx.doi.org/10.1080/09540121.2013.772284. Kiboneka, A., R. J. Nyatia, C. Nabiryo, P. Olupot-Olupot, A. Anema, C. Cooper, and E. Mills. 2008. “Pediatric HIV Therapy in Armed Conflict.” Aids 22: 1097–1098. Kiboneka, A., R. J. Nyatia, C. Nabiryo, A. Anema, C. L. Cooper, K. A. Fernandes, J. S. G. Montaner, and E. J. Mills. 2009. “Combination antiretroviral therapy in population affected by conflict: Outcomes from large cohort in northern uganda.” British Medical Journal 338 (7692) (02/21): 460–463. Kimbrough, William, Vanessa Saliba, Maysoon Dahab, Christopher Haskew, and Francesco Checchi. 2012. “The Burden of Tuberculosis in Crisis-Affected Populations: A Systematic Review.” The Lancet Infectious Diseases 12: 950–965. Mendelsohn, J. B., M. Schilperoord, P. Spiegel, D. A. Ross. 2012. “Adherence to antiretroviral therapy and treatment outcomes among conflict-affected and forcibly displaced populations: A systematic review.” Conflict and Health 6 (9) http://www. conflictandhealth.com/content/6/1/9. Mills, E. J., J. B. Nachega, I. Buchan, J. Orbinski, A. Attaran, S. Singh, B. Rachlis, P. Wu, C. Cooper, L. Thabane, K. Wilson, G. H. Guyatt, and D. R. Bangsberg. 2006. “Adherence to Antiretroviral Therapy in Sub-Saharan Africa and North America: A Meta-Analysis.” The Journal of the American Medical Association 296 (6): 679–690. Mills, E. J., N. Ford, Sonal Singh, and O. Eyawo. 2009. “Providing Antiretroviral Care in Conflict Settings.” Current HIV/AIDS Reports 6 (4): 201–209. National Institue for Health and Clinical Excellence. 2012. The guidelines manual. [cited 03/01 2013]. Available from http://publications.nice.org.uk/the-guidelines-manualpmg6. O’Brien, Daniel P., Sarah Venis, Jane Greig, Leslie Shanks, Tom Ellman, Kalpana abapathy, Lisa Frigati, and Clair Mills. 2010. “Provision of Antiretroviral Treatment in Conflict Settings: The Experience of médecins sans frontières.” Conflict and Health 4 (1): 12–20. Olupot-Olupot, P., A. Katawera, C. Cooper, W. Small, A. Anema, and E. Mills. 2008. “Adherence to Antiretroviral Therapy among a Conflict-Affected Population in Northeastern Uganda: A Qualitative Study.” Aids 22 (14): 1882–1884. Pyne-Mercier, L., G. John-Stewart, B. A. Richardson, N. L. Kagondu, J. Thiga, H. Noshy, N. Kist, and M. H. Chung. 2011. “The Consequences of Post-Election Violence on Antiretroviral HIV Therapy in Kenya.” AIDS Care 23 (5): 562–568. Renzaho, A. M. N. 2007. “Mortality Rates, Prevalence of Malnutrition, and Prevalence of Lost Pregnancies Among the Drought-ravaged Population of Tete Province Mozambique.” Prehospital & Disaster Medicine 22 (1): 26–34.
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Rosen, Sydney, Matthew P. Fox, and Christopher J. Gill. 2007. “Patient Retention in Antiretroviral Therapy Programs in Sub-Saharan Africa: A Systematic Review.” PLoS Med 4 (10) (10/16): e298. Salami, O., A. Buzu, and C. Nzeme. 2010. “High Level of Adherence to HAART Among Refugees and Internally Displaced Persons on HAART in Western Equatorial Region of Southern Sudan.” Journal of the International AIDS Society 13: (4): 123. The Sphere Project. 2011. Humanitarian Charter and Minimum Standards in Humanitarian Response. 3rd ed. The Sphere Project. Unge, C., B. Sodergard, G. Marrone, A. Thorson, A. Lukhwaro, J. Carter, F. Ilako, and A. M. Ekstrom. 2010. “Long-term Adherence to Antiretroviral Treatment and Program Drop-out in a High-risk Urban Setting in Sub-Saharan Africa: A Prospective Cohort Study.” PloS One 5 (10) (Oct 25): e13613. UNHCR, and Southern African HIV Clinicians Society. 2007. Clinical Guidelines for Antiretroviral Therapy Management for Displaced Populations - Southern Africa. Geneva: Southern African HIV Clinicians Society/ UNHCR. Vreeman, Rachel C., Winstone M. Nyandiko, Edwin Sang, Beverly S. Musick, Paula Braitstein, and Sarah E. Wiehe. 2009. “Impact of the Kenya post-Election Crisis on Clinic Attendance and Medication Adherence for HIV-Infected Children in Western Kenya.” Conflict and Health 3 (04/04): 5. Walldorf, J. A., P. Joseph, J. S. Valles, J. F. Sabatier, B. J. Marston, K. Jean-Charles, E. Louissant, and J. W. Tappero. 2012. “Recovery of HIV Service Provision PostEarthquake.” Aids 26 (11): 1431–1436. Yoder, Rachel .B., Winstone M. Nyandiko, Rachel C. Vreeman, Samwel O. Ayaya, Peter O. Gisore, Paula Braitstein, Sarah E. Wiehe. 2012. “Long-term Impact of The Kenya Postelection Crisis on Clinic Attendance and Medication Adherence for HIV-infected Children in Western Kenya.” Journal of Acquired Immune Deficiency Syndromes 59: 199–206.
Appendix: Search Strategy for HIV Treatment Mobile groups 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
HIV Human immunodeficiency Virus Human immunodeficiency virus infection Human immunodeficiency virus agent Acquired immunodeficiency syndrome AIDS or/1–6 drug therapy treatment therapeutics antiretroviral anti-retroviral OR/ 8–12 mobile migrant
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Medicine, Conflict and Survival 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29.
transient refugee displaced internally displaced person asylum seeker Or/14–20 War Conflict Flood Famine Earthquake OR/ 22–26 7 AND 13 AND 21 7 AND 13 AND 27
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Medicine, Conflict and Survival Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/fmcs20
Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review a
Karolina Griffiths & Nathan Ford a
b
Liverpool School of Tropical Medicine , Liverpool , UK
b
Centre for Infectious Disease Epidemiology and Research , University of Cape Town , South Africa Published online: 22 Aug 2013.
To cite this article: Karolina Griffiths & Nathan Ford (2013) Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review, Medicine, Conflict and Survival, 29:3, 198-215, DOI: 10.1080/13623699.2013.813108 To link to this article: http://dx.doi.org/10.1080/13623699.2013.813108
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Medicine, Conflict and Survival, 2013 Vol. 29, No. 3, 198–215, http://dx.doi.org/10.1080/13623699.2013.813108
Provision of antiretroviral care to displaced populations in humanitarian settings: a systematic review Karolina Griffithsa* and Nathan Fordb
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a
Liverpool School of Tropical Medicine, Liverpool, UK; bCentre for Infectious Disease Epidemiology and Research, University of Cape Town, South Africa (Accepted 5 June 2013) Providing antiretroviral treatment (ART) in humanitarian settings is challenging. Reports suggest that ART provision is feasible, but the evidence base is scarce. We systematically searched three databases for studies reporting ART outcomes among displaced populations in settings of conflict, natural disasters or political instability, and estimated overall mortality using random effects models. Fourteen studies were identified, six in conflict areas, five in areas of post-election violence and three in natural disaster settings. The pooled proportion for mortality was 7.6% (95%CI 5.3–10.0%) at six months and 9.0% (95%CI 5.8–12.2%) at 12 months. Loss-to-follow-up at six months was 6.3% (95%CI 4.3–8.3%) and at 12 months was 8.1% (4.9–11.2%). Adherence was comparable to stable settings. Strategies used to support ART provision included additional drug stocks and establishing peer communication networks. Good clinical outcomes can be achieved with ART in disaster setting, in particular if supported by regional collaboration, standardized drug regimens and contingency planning. Keywords: antiretroviral; displaced; humanitarian; HIV; disaster; conflict
Introduction Displaced populations face numerous challenges in accessing antiretroviral therapy (ART), including individual challenges such as transport and loss of income, health service challenges such as disruption to services and drug supplies, and social challenges such as stigma and lack of social support. These challenges, together with the existence of competing health priorities such as malnutrition and tuberculosis, have raised concerns about poor adherence to ART in conflict settings (UNHCR and Southern African HIV Clinicians Society 2007; Olupot-Olupot et al. 2008). Good adherence to ART is essential to ensure optimal health outcomes and limit the development of drug resistance (Esté and Cihlar 2010). *Corresponding author. Email: karolinagriffi[email protected] Ó 2013 Taylor & Francis
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Because of these concerns, international guidance has until recently been hesitant about promoting access to ART in humanitarian emergencies (Ellman, Culbert, and Torres-Feced 2005; The Sphere Project 2011). However, emerging evidence suggests that ART provision is feasible in conflict and disaster humanitarian settings (Kiboneka et al. 2009; O’Brien et al. 2010), and more recent guidelines published by UNHCR and SPHERE have acknowledged the need to provide ART to displaced populations (UNHCR and Southern African HIV Clinicians Society 2007; The Sphere Project 2011). This systematic review summarizes the evidence regarding the effectiveness of ART care in conflict and disaster settings and identifies strategies to support ART adherence in these unstable settings. Methods A systematic literature search was undertaken in PubMed and EMBASE from inception to 1 April 2013 combining key search terms (see Appendix). We additionally screened abstracts of all conferences of the International AIDS Society up to July 2012. Published articles were screened by title and abstract by one author (KG) and agreement on final inclusions was made in duplicate (KG, NF). Searches were limited to English language publications. The bibliographies of full text articles were searched for potentially relevant articles. Studies were selected according to pre-defined inclusion criteria which sought original research articles reporting ART outcomes among HIV positive adults and children who had been displaced due to a humanitarian crisis (defined as conflict, natural disaster or political instability). The primary outcome was mortality and secondary outcomes included virological suppression, CD4 gain, development of drug resistance, adherence (as defined by the studies) loss to follow up, and missed appointments (as defined by the studies). We assessed study quality based on study design, selection or measurement bias, standard case definitions used, follow up of patients, whether confounders were controlled/adjusted and if confidence intervals were provided; this assessment was based on guidelines from the National Institute for Health and Clinical Excellence in the United Kingdom (National Institute for Health and Clinical Excellence 2012), which has been used by other systematic reviews of health challenges in conflict (Kimbrough et al. 2012). No study was excluded on the basis of poor methodological quality. For the primary outcomes of mortality and lost to follow-up we calculated point estimates and 95% confidence intervals for the proportion of patients who had died at different time points. Proportions were stabilized through arcsine square-root transformation and pooled using a DerSimonian–Laird random effects model. All analyses were done in Stata version 12.0.
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Results Characteristics of included studies After screening 6457 titles, fourteen studies were included in this review (Figure 1). Six studies were carried out in armed conflict settings (Kiboneka et al. 2008; Garang, Odoi, and Kalyango 2009; Kiboneka et al. 2009; O’Brien et al. 2010; Salami, Buzu, and Nzeme 2010; Autino et al. 2012). Two studies (Culbert et al. 2007, Vreeman et al. 2009) reported results that were reported by other included studies (O’Brien et al. 2010; Yoder et al. 2012) and were excluded from the final review. Five studies reported outcomes in a setting of post-election violence (Unge et al. 2010; Pyne-Mercier et al. 2011; Bamrah et al. 2013; Doumbouya et al. 2012; Yoder et al. 2012); these studies were undertaken mainly in sub Saharan African, where both HIV and conflicts are most prevalent (Mills et al. 2009), including Kenya, Northern Uganda and the Ivory Coast. Three studies reported outcomes from natural disaster settings (Bhakeecheep et al. 2012; PUBMED 3527 titles & abstracts screened
EMBASE 1735 titles & abstracts screened
IAS Abstracts screened 1195
All References screened
Read in full: 22
Read in full: 13
Read in full: 61
Read in full: 3
Excluded: - 59 (not relevant)
Excluded: - 1 (Culbert 2007) as data reported by another study
Included: 2
Included: 2
13 Excluded as did not fit inclusion criteria: - 3 studies not in crises situation - 2 studies not on ART - 1 study looked at access not provision - 2 discussed organisational issues - 2 case studies not original research - Yoder et al. data replicates Vreeman et al -1 study had qualitative data only - 1 study, no denominator of data
Excluded: - 2 duplicates Seven did not fulfil inclusion criteria: - 2 studies no data on ART - 1 study not original research article - 1 study, no recent data post disaster - 3 studies included migrant workers not in crises situation
Included: 9
Included: 4
3 duplicates
Final Number of articles for inclusion: 14
Figure 1.
Search Strategy.
Snapshot.4 days for adherence.
3 months (22/09/1121/12/11)
Post-election violence
Flooding crisis
Post-election crisis
Armed Conflict
Flooding crisis
Bamrah et al. 2013
Bhakeecheep et al. 2012
Doumbouya et al. 2012
Garang, Odoi, and Kalyango 2009
Khawcharoenporn et al. 2013
Jan-June 2011
6 months. JulyDecember 2011
Survey. One interview day, 10 weeks after election
4 years, 7 months (01/01/ 07- 15/08/11)
Political crisis/ migrant workers from conflict
Autino et al. 2012
Reporting period
Type of crisis
Summary table of study characteristics.
Author
Table 1
Rural district, in CentralWest Burkina Faso 3 provinces in Kenya, Rift Valley, Nyanza, Central 22 provinces in Lower North and Central Thailand 5 health regions in conflict in Ivory Coast Urban, IDP camp and surrounding area, Gulu, Northern Uganda Central Thailand
Study setting
1.20% (UNAIDS)
6.5 % (UNAIDS 2009)
3% (UNAIDS, Adults)
1.20% (UNAIDS)
6.7% (national)
1.3% in rural district of Burkina Faso
Estimated regional/national HIV prevalence at time of study
HIV clinic at large referral hospital
Lacor Hospital,
68 healthcare centres
35 health facilities providing ART and 9 IDP camps 242 Hospitals
Nanoro District Hospital
Place of care Age (years)
Unclear
Missionary not- for – profit organisation
NGOAconda
Government
40
Unclear
NR
NR
Government 40 and European ESTHER alliance Not clear 37 years, 39.1 in IDP camps
Provider
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(Continued)
45% (97/217)
67.5 % (135/200)
NR
NR
70%, 64% in IDP camps
40.3% (56/139)
Female (%)
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12 months
Armed conflict or post conflict settings
Post election violence
O’Brien et al. 20101
Pyne-Mercier et al. 2011
Armed conflict
Snapshot, Feb 2008.
Armed Conflict
Kiboneka et al. 2008
2 months. 30/12/2007 -28/02/2008
2 years, 7 months (8 June 2005 – 29 Jan 2008)
Armed conflict
Kiboneka et al. 2009
Reporting period
Type of crisis
Author
Table 1. (Continued).
Western equatorial
Urban IDP camp and surrounding area, Gulu Northern Uganda Urban IDP camp and surrounding area, Gulu Northern Uganda. 12 programmes11 Sub Saharan Africa, 1 India. Most rural. 2 refugee camps. Nairobi
Study setting
12.1% (regional)
7.8%
1- 10 %
6.5% (UNAIDS 2009)
6.5% (UNAIDS 2009)
Estimated regional/national HIV prevalence at time of study
HIV clinic
One HIV clinic
Clinics and hospitals.
District hospital.
Lacor Hospital,
Place of care
Faith based Not-for-profit organisation, funded by PEPFAR International organisations,
NGO (MSF)
Missionary not for profit organisation.
Missionary not- for – profit organisation
Provider
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NR
37
35
8
39
Age (years)
NR
(Continued)
63.8% (1617/ 2534)
66%
60% (34/57)
72% 1162/1625
Female (%)
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Postelection violence
Yoder et al. 2012
14 months (26/10/200731/12/2008)
5 months post earthquake (12 January May 2010)
9 months. July 2009-March 2010 1 month (01.01.200801.02.2008)
Urban and rural, Western Kenya
state Southern Sudan Informal urban settlement, Kibera, Nairobi, Kenya Rural and urban, Haiti
Study setting
7.8% (Adults and children)
1.9%
7.8%
African Medical Research Foundation
supported by WHO
Provider
50 PEPFAR Ministry of supported public health, sites international and national NGOs. One urban AMPATH2 referral hospital,26 urban and rural clinics, 23 satellite clinics
One HIV Clinic
Place of care
NR
50.2% (1269 of 2549 children on or off ART)
Unclear for those on ART
NR
Female (%)
NR
NR
Age (years)
Notes: 1O Brien et al includes data from separate studies.2AMPATH – USAID-Academic Model Providing Access to Healthcare clinical care system, a joint initiative between Indiana University School of Medicine, Moi University School of Medicine, Kenya and Moi Teaching and Referral Hospital.
Post-earthquake
Postelection violence
Salami, Buzu, and Nzeme 2010 Unge et al. 2010
Reporting period
Estimated regional/national HIV prevalence at time of study
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Walldorf et al. 2012
Type of crisis
Author
Table 1. (Continued).
Medicine, Conflict and Survival 203
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Walldorf et al. 2012; Khawcharoenporn et al. 2013). Finally, two studies only reported results for children (Kiboneka et al. 2008; Yoder et al. 2012). Four studies were supported by non-governmental organizations and four sites were run by faith-based organizations (Table 1). All programmes provided ART free of charge. The average age of adults in the studies ranged from 35–40 years and for children was 8 years. Of the studies that reported sex of participants, the majority (7/9) included more women than men. Baseline CD4 counts ranged from 97–224 cells/mm3.
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Assessment of study quality All of the included studies were observational cohorts. Three of the studies were published as abstracts, and did not provide enough information to fully assess the study methodology (Salami, Buzu, and Nzeme 2010; Doumbouya et al. 2012; Bhakeecheep et al. 2012). Nine of the studies did not statistically adjust for confounders and seven studies did not follow up patients for more than six months. Two studies were given a ‘higher rating’ of overall strength of study quality (Kiboneka et al. 2009; Yoder et al. 2012), five studies were given a ‘medium’ rating, (Garang, Odoi, and Kalyango 2009; O’Brien et al. 2010; Autino et al. 2012; Walldorf et al. 2012; Khawcharoenporn et al. 2013) and seven studies a ‘lower’ rating (Kiboneka et al. 2008; Salami, Buzu, and Nzeme 2010; Unge et al. 2010; Pyne-Mercier et al. 2011; Bamrah et al. 2013; Bhakeecheep et al. 2012). (See Supplementary Table 1 available on the publisher’s website at http://dx.doi.org/10.1080/13623699.2013.813108) ART outcomes Three studies reported mortality data from 14 cohorts across seven countries. Mortality at six months ranged from 1.0% (95%CI 0.9–8.2%) to 28.3% (95% CI 11.7–37.1%) with a pooled proportion of 7.6% of patients having died (95%CI 5.3–10.0%). Mortality at 12 months ranged from 2.6% (95%CI 2.2–20.6%) to 28.0% (95%CI 9.5–51.8%) with a pooled proportion of 9.0% of patients having died (95%CI 5.8–12.2%). (Figure 2.) Loss to follow up was reported by three studies (14 cohorts) and the pooled proportion was 6.3% (95%CI 4.3–8.3%) at six months and 8.1% (4.9–11.2%) at 12 months. CD4 gain was reported by two studies (Table 1). Changes in six month CD4 counts ranged from 129–187 cells/mm3. Adherence, reported by six studies, was over 80% in all settings, with four studies reporting adherence rates of over 90%, (Kiboneka et al. 2008; Garang, Odoi, and Kalyango 2009; Kiboneka et al. 2009; Yoder et al. 2012). Missed appointments were reported in seven studies using different definitions over varying time periods (Table 1). In settings of political crisis, 4.7–11% of patients missed appointments in Kenya and 16.1% described
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Setting
Proportion (95% CI) n
Duration
205
e
6 months 6 months CAR Bogulia Cote d'Ivoire, Danane 6 months 6 months DRC, Dubie 6 months DRC, Kilwa 6 months DRC, Baraka 6 months DRC, Bukavu 6 months DRC, Walikale 6 months India, Manipur 6 months RoC, Kindamba 6 months RoC, Kinkala 6 months RoC, Mindoull 6 months Uganda Kitkum Subtotal
6.60 (1.97, 13.66) 6.13 (4.17, 8.45) 28.32 (13.91, 45.47) 23.16 (11.70, 37.12) 15.53 (8.24, 24.61) 8.00 (6.66, 9.45) 0.97 (0.87, 8.23) 4.09 (2.79, 5.63) 19.37 (4.97, 40.19) 16.64 (6.10, 31.02) 6.02 (3.10, 9.82) 8.22 (3.22, 15.24) 7.62 (5.29, 9.96)
67 480 29 40 73 1443 25 745 17 32 190 78
4 29 8 9 11 115 0 30 3 5 11 6
12 months 12 months CAR Bogulia Cote d'Ivoire, Danane 12 months 12 months DRC, Dubie 12 months DRC, Kilwa 12 months DRC, Baraka 12 months DRC, Bukavu 12 months DRC, Walikale 12 months India, Manipur 12 months RoC, Kindamba 12 months RoC, Kinkala 12 months RoC, Mindoull 12 months Uganda Kitkum Subtotal
6.19 (0.93, 15.63) 8.99 (6.14, 12.32) 28.07 (9.50, 51.80) 27.13 (13.91, 42.84) 18.26 (9.05, 29.80) 11.05 (9.39, 12.81) 1.82 (1.60, 14.96) 4.14 (2.74, 5.82) 2.57 (2.20, 20.57) 6.70 (5.12, 46.64) 8.40 (4.20, 13.87) 14.96 (4.69, 29.67) 9.00 (5.75, 12.24)
39 327 15 34 51 1289 13 639 9 3 124 29
2 29 4 9 9 142 0 26 0 0 10 4
NOTE: Weights are from random effects analysis -51.8
0
51.8 Percentage
Figure 2.
Pooled proportion for mortality.
treatment interruptions. Service delivery was a concern with almost a half of centres in the Ivory Coast failing to deliver ART. No studies reported virological suppression as an outcome. No studies reported development to drug resistance, although one abstract highlighted the need to monitor drug resistance throughout ART programmes (Bhakeecheep et al. 2012). Within natural disaster settings patient retention was high. During floods in Thailand 10% (4167/41,673) of patients had missed one appointment or more (Bhakeecheep et al. 2012). Only 7/217 HIV patients on ART at one HIV clinic in Thailand reported no access to treatment during the disaster (Khawcharoenporn et al. 2013). Walldorf et al. (2012) reported that 97% of current patients on ART from the baseline pre-earthquake were followed up in the following four months post-earthquake. This was reduced to 90.5% in areas that were affected most by the earthquake; however the ART programme continued to enrol patients five months post earthquake.
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Strategies to support ART delivery A range of strategies were reported by the studies to support ART delivery, including regional collaboration between other HIV care services, patient education and adherence counselling, standardized drug regimens/treatment protocols, establishing a communication network between patients, and provision of additional medication stock to patients in case of crisis (Table 2). One study reported that decentralization of ART services may improve access (Pyne-Mercier et al. 2011). Another study (Autino et al. 2012) established a formal international transfer process between sites in Burkina Faso and the DRC, an example of effective continuity of care. Patient follow up within humanitarian settings is complicated by disrupted transport facilities and security concerns. Proposed solutions reported by the studies in this review included extending peer networks, using computerized record keeping to highlight when drug refills are necessary (Unge et al. 2010), peer ART delivery (Bhakeecheep et al. 2012), and mobile telephones to aid with follow up of patients (Autino et al. 2012; Bamrah et al. 2013; Walldorf et al. 2012) and sending adherence reminders (Bhakeecheep et al. 2012). In Thailand, reducing restrictions on second line regimens was recommended (Bhakeecheep et al. 2012). Other authors recommended ensuring drug regimens are standardized across the region in case of population displacement (O’Brien et al. 2010). The importance of disaster preparedness and collaborative activities between patients, healthcare providers and government was highlighted, with Khawcharoenporn et al. (2013) separating strategies into preflood, flood and post-flood period. Discussion The effectiveness of ART is well established, and the extent to which good treatment outcomes can be achieved in disaster settings depends on a range of delivery challenges including continuity of drug supply, innovative approaches to supporting patient adherence, and access to services for patients and health staff to dispense drugs. Our review found that overall ART outcomes were satisfactory. Mortality, loss-to-follow-up, and adherence were all within the range reported by ART programmes in stable programmes in resource-limited settings (Braitstein et al. 2006; Mills et al. 2006; Rosen, Fox, and Gill 2007). These findings are consistent with those reported by a recent review of antiretroviral adherence in conflict-affected and forcibly displaced populations which reported satisfactory levels of adherence compared to non-affected groups (Mendelsohn et al. 2012). Only 14 studies were eligible for inclusion in this review, despite using a broad search criteria that resulted in an extensive search of both published literature and conference abstracts. This limitation in the evidence base may be due to the difficulties and challenges of undertaking research in conflict and
139 migrant workers returning from Demoncratic Republic of Congo (134), Ghana (3) and France (2). 107 on ART
1’294 facility based respondents, 336 IDPs
41’673 PLWHA receiving ART in 242 hospitals 17’471 PLWHA receiving ART in 68 centres 200 Adults (>18)
Autino et al. 2012
Bamrah et al. 2013
Bhakeecheep et al. 2012
Garang, Odoi, and Kalyango 2009
Doumbouya et al. 2012
Participants
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
Missed appointments (varied methods of reporting)
NR
NR
NR
NR
(Continued)
4167/ 41,673 (10%) had 1 missed appointment or more 32/68 (47%) centres failed to deliver ART
4.7% (rift valley), 6.8% (Nyanza), 11% (Central province) not returned to routine health care facilitiy since post election unrest
14/107 (13.1%) NR over 43 months.10.2 per 100 patients per year
Loss to follow up (varied time periods recorded)
NR 99.6% Adherence amongst IDPS (>95% adherence levels over 4 days, self reports) compared to 99.5% Non IDPs
NR
During Jan 2008:31 (17.6%) in Rift Valley, 24 (9.3%) in Nyanza, 9 (4.8%) in Central province of patients reported missing therapy.83.6 (Rift Valley), 42.9 (Nyanza), 28.9 (Central) therapy days missed per 1000 NR
NR
NR
Virological CD4 cell suppression count Baseline: 224 (+/– 184)After 6 months: 411 (+/– 305)Mean gain of 187 cells/mm3 NR
Drug resistance development Adherence
NR
16/107 (15%) over 4 years, 7 months. 11.6 per 100 patients per year
Mortality
Summary table of study outcomes.
Author
Table 2.
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Participants
217 adults
1625 Adults
57 Children
4145 adults2572 with 12 month data
2534 adult patients
159 adults
722 patients
Author
Khawcharoenporn et al. 2013
Kiboneka et al. 2009
Kiboneka et al. 2008
O’Brien et al. 2010
Pyne-mercier et al. 2011
Salami, Buzu, and Nzeme 2010
Unge et al. 2008
Table 2. (Continued).
NR
NR
NR
9% Mortality of those on ART, 12 months.
Mortality rate: 69/ 1625 (4.2%) from 08/06/2005 to 29/ 01/2008Mortality Incidence Rate: 3.48 (95% CI 2.66 to 4.31) per100 person years NR
NR
Mortality
NR
NR
NR
Mean baseline: 97 cells/ mm3
Median baseline: 139 cells/ mm3Median gain at 6 months: 129 cells/ mm3 NR
NR
NR
NR
Baseline: median 144 cells/mm3 Baseline median: 157 (90–220)
NR
NR
NR
Virological CD4 cell suppression count
NR
NR
NR
NR
90/102 (88%) reported adherence levels > 95% (missed less than 3 doses in past month) NR
NR
92.2% had good adherence (>95% combination ART adherence, measured by pharmacy monitored drug possession ratio, pharmacy refill records and 3 day recall report) 92% had good adherence (>95% adherence) NR
NR
NR
NR(only pre flood data)
NR
Drug resistance development Adherence
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NR
NR
NR
466/2572 (11%)
(Continued)
186 of 447 (42%) of scheduled appointments were missed
408/2534 (16.1%) experienced treatment interruptions NR
NR
NR
NR
NR
7/217 (3%) self reported no access to ART during study period NR
Missed appointments (varied methods of reporting)
NR
Loss to follow up (varied time periods recorded)
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24,863 patients on ART baseline December 2009.
1627 children under the age of 14 on ART
Walldorf et al. 2012
Yoder et al. 2012
Note: NR = not reported.
Participants
Author
Table 2. (Continued).
NR
NR
NR
NR
Mortality
NR
NR
Virological CD4 cell suppression count
NR
NR
91.8% (1’494/1627) had perfect adherence (defined as taken “all” pills in past 7 days) 4 months post election and 91% (1481/1627) had perfect adherence 5-10 months post election
NR
Drug resistance development Adherence
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3% (49/1627) initial loss to follow up, 2.6% (42/1627) after 12 months
NR
Loss to follow up (varied time periods recorded) 3% fewer patients attended clinical examination visit for ART 3 months post earthquake. 3.9% increase from baseline 4 months post earthquake. NR
Missed appointments (varied methods of reporting)
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disaster settings. Only three studies reported outcomes of ART delivery in natural disasters, despite the evident need to continue to address ART provision in these difficult circumstances. For example, a study from Tete province in Mozambique during prolonged drought highlighted the need to align food aid and HIV programmes (Renzaho 2007); however, this study did not report outcomes that could allow for its inclusion in this review. Several recommendations to improve ART in displaced populations in humanitarian settings emerge from this review. Key issues include contingency planning and coordination between organizations to ensure continuity of care. It is necessary to bridge ART between emergency aid in relief situations and in the development phase to ensure long-term use. Improved collaboration between non-governmental organizations (NGO) and the private services may allow patients to access ART from a greater range of health facilities (Unge et al. 2010). Patients were reported to receive ART and care from other provider sites, but may not have medical notes detailing these visits (Vreeman et al. 2009). Healthcare providers should keep up-to-date lists to inform patients of alternate regional clinic sites and pharmacies during an emergency (Walldorf et al. 2012). Contingency planning has been shown to be effective in improving adherence (Culbert et al. 2007). Despite the risk of medications being lost or sold, it is necessary to consider providing medication for extended periods when violence or political instability is predicted (Unge et al. 2010). Busy periods may be predicted, for example post-election periods or where rising tensions are documented between groups known to be associated with violence and conflict, and ART providers should recognize this and ensure contingencies are put in place (Pyne-Mercier et al. 2011). Certain ‘at-risk populations’ may have increased difficulties during a crisis, it is vital to understand the political ethnic compositions of a region in order to optimize care (Yoder et al. 2012). Some study sites reduced non-essential services to a minimum in order to prioritize and successfully continue ART provision (O’Brien et al. 2010; Doumbouya et al. 2012). This review has several limitations to note. The database search was only run in English, and studies published in other languages may exist. Publication bias may be a concern, as organizations may be less willing to report negative outcomes, and risk of bias is a concern given that all studies were observational and the majority were rated as medium or low quality. Many of the studies were from well-supported sites that received external support from international agencies, and outcomes may be different in contexts where such additional support is lacking. Finally, most studies in this review came from conflict settings in sub-Saharan Africa, and challenges and solutions may be different in other contexts. Organizations involved in the provision of ART in humanitarian settings are encouraged to report their approaches and outcomes, particularly in response to natural disasters, as these are under-represented in the literature.
X X
X
X
X X
X
X
X
X
X X
Additional drug stocks for patients
X
X
Standardize drug regimens/ treatment protocols
X
X X
Good collaboration with regional health services/ NGOs
X
X
Duplicate medical records
X X
X
X X
X
X
X
X
X
X
Patient education and adherence counselling
X
X
X
X
X
Electronic Medical Follow up Record outreach System programme
Strategies recommended to improve care in displaced populations in humanitarian settings.
Autino et al. 2012 Bamrah et al. 2013 Bhakeecheep et al. 2012 Doumbouya et al. 2012 Khawcharoenporn et al. 2013 Kiboneka et al. 2009 O’Brien et al. 2010 Pyne-Mercier et al. 2011 Salami, Buzu, and Nzeme 2010 Unge et al. 2010 Vreeman et al. 2009 Walldorf et al. 2012
Table 3.
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X
X
X
X
X
X X
X
X
X
X
Communication Networks with Task Operational Patients Shifting research
Medicine, Conflict and Survival 211
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In conclusion, despite a clear recognition of the need to ensure continuity of care for people living with HIV affected by humanitarian disaster there remains a lack of reporting on approaches to improve the effectiveness of ART in humanitarian settings. Nevertheless, outcomes are generally encouraging, and demonstrate that with approaches such as improved collaboration, standardized drug regimens and improved preparedness it is possible to achieve the same outcomes in humanitarian settings as in stable settings. Acknowledgements
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The authors would like to acknowledge Timothy O’Dempsey for his advice and support.
Supplemental data Supplemental data for this article can be accessed here: http://dx.doi.org/ 10.1080/13623699.2013.813108 Notes on contributors Karolina Griffiths is a Royal Liverpool University Hospital foundation doctor, a graduate of the University of Liverpool and the Liverpool School of Tropical Medicine. Nathan Ford is a research associate at the University of Cape Town with a special interest in the delivery of antiretroviral therapy in resource-limited settings.
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Appendix: Search Strategy for HIV Treatment Mobile groups 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
HIV Human immunodeficiency Virus Human immunodeficiency virus infection Human immunodeficiency virus agent Acquired immunodeficiency syndrome AIDS or/1–6 drug therapy treatment therapeutics antiretroviral anti-retroviral OR/ 8–12 mobile migrant
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transient refugee displaced internally displaced person asylum seeker Or/14–20 War Conflict Flood Famine Earthquake OR/ 22–26 7 AND 13 AND 21 7 AND 13 AND 27
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