Article Text

Availability, cost and affordability of essential medicines for chronic respiratory diseases in low-income and middle-income countries: a cross-sectional study
  1. Marie Stolbrink1,2,
  2. Obianuju B Ozoh3,4,
  3. David M G Halpin5,
  4. Rebecca Nightingale2,
  5. Jamilah Meghji6,
  6. Catherine Plum7,
  7. Brian William Allwood8,9,
  8. Shamanthi Jayasooriya10,
  9. Kevin Mortimer11,12,13
  10. Chronic Respiratory Diseases Medicines Survey Investigators Collaboration
    1. 1 Clinical Sciences, Stellenbosch University, Stellenbosch, South Africa
    2. 2 Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, UK
    3. 3 Department of Medicine, University of Lagos College of Medicine, Lagos, Nigeria
    4. 4 Department of Medicine, Lagos University Teaching Hospital, Surulere, Nigeria
    5. 5 Department of Respirology, Royal Devon and Exeter Hospital, Exeter, UK
    6. 6 Imperial College London, London, UK
    7. 7 University Hospitals of Morecambe Bay NHS Trust, Kendal, UK
    8. 8 Department of Pulmonology, Tygerberg Academic Hospital, Cape Town, South Africa
    9. 9 Department of Pulmonology, Stellenbosch University Faculty of Medicine and Health Sciences, Cape Town, South Africa
    10. 10 Academic Unit of Primary Care, The University of Sheffield, Sheffield, UK
    11. 11 Department of Medicine, University of Cambridge, Cambridge, UK
    12. 12 Department of Medicine, University of KwaZulu-Natal College of Health Sciences, Durban, South Africa
    13. 13 Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
    1. Correspondence to Dr Marie Stolbrink, Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK; mstolbrink{at}doctors.org.uk

    Abstract

    Contemporary data on the availability, cost and affordability of essential medicines for chronic respiratory diseases (CRDs) across low-income and middle-income countries (LMICs) are missing, despite most people with CRDs living in LMICs. Cross-sectional data for seven CRD medicines in pharmacies, healthcare facilities and central medicine stores were collected from 60 LMICs in 2022–2023. Medicines for symptomatic relief were widely available and affordable, while preventative treatments varied widely in cost, were less available and largely unaffordable. There is an urgent need to address these issues if the Sustainable Development Goal 3 is to be achieved for people with asthma by 2030.

    • Asthma
    • COPD Pharmacology
    • Asthma Pharmacology
    • Health Economist
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    Introduction

    The forthcoming High-Level Meeting of the United Nations General Assembly on Non-Communicable Diseases (NCDs) will address the 15 million premature deaths from NCDs annually, most of which occur in low-income and middle-income countries (LMICs).1 The United Nations Sustainable Development Goals (SDGs) demand ‘safe, effective, quality and affordable essential medicines for all’ by 2030.2 Non-communicable chronic respiratory diseases (CRDs), for example, asthma and chronic obstructive pulmonary disease (COPD), cause substantial morbidity and mortality, disproportionately affecting those living in poverty in LMICs.3 Recommended medicines for CRDs include inhaled and oral drugs that are on the WHO Model List of Essential Medicines (EML), which defines safe, efficacious, cost-effective medicines that should be available everywhere.4 Access to essential, affordable CRD medicines is limited in LMICs.5 6 Up-to-date data on the availability, cost and affordability of WHO essential medicines for CRDs in LMICs are missing.

    Methods

    This cross-sectional survey of medication availability and cost was completed by healthcare professionals working in LMICs (online supplemental appendix). Professionals collected standardised data from three facilities (pharmacy, healthcare facility (HCF) and central medicine store (CMS)) in each country. Prices (US$) for 1-month treatment were compared. Affordability was defined by 1-month treatment costing the lowest paid government worker <1 day’s wage, as per established methodology.7

    Supplemental material

    Results

    Data from 60 LMICs were collected between June 2022 and April 2023 (online supplemental appendix). 18 countries were low income, 24 lower middle income and 17 upper middle income. The sub-Saharan African region was best represented (27 countries). Information for all three facilities was submitted for 42/60 (70%) countries. Information for pharmacies, HCFs and CMS was provided by 57, 56 and 46 LMICs, respectively. Most pharmacies were private (89%), most HCFs were public institutions (80%).

    Inhaled short-acting beta agonists

    Inhaled short-acting beta agonist (SABA) was available in 93% of pharmacies, 79% of HCFs and 78% of CMS (table 1, figure 1, online supplemental appendix). The median cost of 1-month treatment in pharmacies was $2.95 (IQR $1.99–4.97), $2.34 (IQR $1.38–3.86) in HCFs and $1.39 (IQR $1.20–2.83) in CMS. SABAs were both available and affordable in 51% (29/57) of all pharmacies and 61% (31/56) of all HCFs that submitted data.

    Table 1

    Comparisons of availability and costs for 1-month treatment for standardised SABA, ICS, ICS-LABA and LAMA formulations in pharmacy, HCF and CMS

    Figure 1

    Availability and affordability of standardised (A) SABA, (B) ICS, (C) ICS-LABA (100+6 mcg/dose), (D) ICS-LABA (200+6 mcg/dose) and (E) LAMA formulations in pharmacy or HCF. Blue: available and affordable. Yellow: available but not affordable. Orange: unavailable. Grey: low-income and middle-income country (LMIC), no information. HCF, healthcare facility; ICS, inhaled corticosteroid; ICS-LABA, inhaled corticosteroid–long-acting beta agonist (formoterol) combination; LAMA, long-acting muscarinic antagonist inhaler; SABA, short-acting beta agonist inhaler.

    Inhaled corticosteroids

    Beclomethasone 100 mcg/dose, or equivalent, was available in 54% of pharmacies, 55% of HCFs and 48% of CMS (table 1, figure 1, online supplemental appendix). The median costs were $5.40 (IQR $2.12–8.60) in pharmacies, $3.01 (IQR $1.21–5.89) in HCFs and $1.16 (IQR $0.11–3.24) in CMS. Inhaled corticosteroids (ICS) were both available and affordable in 30% (17/57) of pharmacies and 36% (20/56) of HCFs.

    Combination inhaled corticosteroid–long-acting beta agonists

    Budesonide-formoterol 200+6 mcg/dose, or equivalent, was available in 54% of pharmacies, 38% of HCFs and 20% of CMS (table 1, figure 1, online supplemental appendix). The median costs were $19.20 (IQR $9.73–27.43) in pharmacies, $18.41 (IQR $11.30–24.49) in HCFs and $7.14 (IQR $3.90–8.13) in CMS. Overall, it was both available and affordable in 11% (6/57) of pharmacies and 5% (3/56) of HCFs. Costs for budesonide-formoterol 100+6 mcg/dose were similar, but it was less available.

    Long-acting anti-muscarinic antagonists

    A standardised long-acting muscarinic antagonist (LAMA) formulation was available in 46% of pharmacies, 29% of HCFs and 24% of CMS (table 1, figure 1, online supplemental appendix). The median costs were $30.53 (IQR $9.45–47.29) in pharmacies, $26.01 (IQR $15.32–36.70) in HCFs and $17.98 (IQR $0.98–32.17) in CMS. LAMAs were available and affordable in 7% (4/57) of pharmacies and 4% (2/56) of HCFs.

    Other essential medicines, WHO regions and income groups

    Oral prednisolone was affordable and available between 70% and 80% of facilities (table 1). Other medicines were less available (online supplemental appendix). There were variations which region and income groups had the cheapest and most affordable medicines across facilities.

    Discussion

    This is the largest cross-sectional study of availability, cost and affordability of CRD medicines in LMICs to date. It included data from 60 LMICs, representing 84% of the global LMIC population, and 16 of the 20 most populous LMICs.

    Inhaled SABA and prednisolone were almost universally available. There were large cost ranges, SABAs were the cheapest inhalers. Medicines were cheaper in HCFs than pharmacies and price typically increased between CMS and pharmacy/HCF. In some countries medicines were free or subsidised.

    We identified improvement in inhaled corticosteroid–long-acting beta agonist (ICS-LABA) availability compared with the last decade, with ICS-LABA now being available in more than half of pharmacies, and one-third of HCFs, possibly because of inclusion in the WHO EML and international guidelines.6 SABA and ICS availability in HCFs and CMS also improved compared with previously.5

    Acute, symptomatic treatments (SABA, prednisolone) for CRDs were more affordable than daily treatments needed to reduce morbidity and mortality (ICS, ICS-LABA, LAMA). Guidelines recommend that first-line asthma treatment should be ICS-LABA, or ICS whenever SABA is taken.8 However, our findings suggest that these recommendations are largely unaffordable, and economic realities may force patients to use cheaper, riskier approaches.8

    The median daily wage was $4.33 (IQR $2.17–9.55) providing an indication of ‘affordability’ for a month’s treatment, but acknowledging that many earn less than the lowest paid government worker. Making ICS-formoterol (median cost at least $16.49) affordable like this, or by benchmarking against SABA, could achieve a tipping point for the widespread adoption of anti-inflammatory reliever asthma therapy, especially considering the greater efficacy of ICS-formoterol.8 A similar approach to LAMA pricing could improve COPD management.9

    Our study had several strengths. Data came from all income levels and regions and represented a large proportion of those living in LMICs. Comparisons were possible by using standardised data collection derived from established tools. Patient experience was reflected, as we presented a snapshot of the facility on the data collection day.

    The study had some weaknesses. It was conducted over 11 months. Costs were compared using US$, dependent on exchange rates. Median price ratios were previously used for benchmarking, but the reference prices are out of date and no longer recommended.7 Convenience sampling introduced possible selection bias towards better equipped facilities in urban areas. Mostly only one facility was sampled per country. We did not assess medicine quality, expiry date nor data from multiple time points.

    Establishing national CRD strategies that include medicines, generating country-specific data, buy-in from global organisations and patient advocacy are key to improving medicine access by addressing in-country demand and political commitment.10 Cost-effectiveness data for inhaled medicines specific for LMICs are needed, given that they reduce exacerbations and hospitalisations, which substantially drive the costs of CRDs.9 There is an urgent need to address the availability and affordability of essential CRD medicines if SDGs are to be achieved for all by 2030.

    Ethics statements

    Patient consent for publication

    Ethics approval

    Investigators gave informed consent and gained local approvals where necessary. This questionnaire for professionals with objective responses was sponsored by Liverpool School of Tropical Medicine (21-039).

    References

    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • X @de_shami

    • Collaborators Eris Mesonjesi (University Hospital Center Mother Teresa, Tirana, Albania), Nadia Ait-Khaled (Algeria University, Algeria), Samya Taright (Universite d’Alger, Faculté de Medecine, Algeria), Santiago Larrateguy (Universidad Adventista del Plata/Centro Privado de Medicina Respiratoria, Argentina), Sanela Domuz Vujnovic (Paediatrics Clinic, University Clinical Center of Republic of Srpska, Bosnia and Herzegovina), Carolina Barbosa Souza Santos (Programa para o Controle da Asma na Bahia-ProAR (Program for Control of Asthma in Bahia), Brazil), Abdoul Risgou Ouédraogo (Health Training & Research Unit, Joseph KI-ZERBO University, Ouagadougou, Burkina Faso and Department of Medicine, Tengandogo University Hospital Center, Burkina Faso), Bertrand Hugo Mbatchou-Ngahane (Douala General Hospital, University of Douala, Cameroon), Lydie Mboumi (Pharmacie du Rocher, Douala, Cameroon), Yanping Liu (Sun Yat-sen University, China), Fu-Qiang Wen (West China Hospital, Sichuan University, China), Xi Yan (West China Hospital, Sichuan University, China), Yutian Zhang (West China Hospital, Sichuan University, China), Patrick Katoto (Center for Tropical Diseases and Global Health, Université Catholique de Bukavu, Congo, Democratic Republic), Arsene Daniel Nyalundja (Center for Tropical Diseases and Global Health, Université Catholique de Bukavu, Democratic Republic of Congo), Efraín Sánchez-Angarita (Centro de Investigacion Respiratorio, Ecuador), Maged Hassan (Alexandria University Faculty of Medicine, Egypt, Arab Republic), Magda Afifi (National Tuberculosis Control Program, Ministry of Health and Population, Egypt, Arab Republic), Willie Siduna (University of the Western Cape, Eswatini), Amsalu Binegdie (College of Health Sciences, Addis Ababa University, Ethiopia), Babatunde Awokola (Liverpool School of Tropical Medicine and Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Gambia, The Rafiuk Cosmos Yakubu, Tamale Teaching Hospital (TTH) and School of Medicine, University for Development Studies (UDS), Ghana), Magassouba Aboubacar Sidiki (National Tuberculosis Control Program, Conakry, Guinea), Suyapa Sosa (Pulmonary Medicine/Thorax National Institute, Honduras), Sarbjeet Khurana (IHBAS Hospital, India), Bony Wiem Lestari (Research Center for Care and Control of Infectious Diseases (RC3ID), Universitas Padjadjaran, Bandung, Indonesia), Faisal Yunus (Department of Pulmonology and Respiratory Medicine, Faculty of Medicine Universitas Indonesia, Persahabatan Hospital, Indonesia), Antonia Morita Iswari Saktiawati (Universitas Gadjah Mada, Faculty of Medicine, Public Health, and Nursing, Department of Internal Medicine, Indonesia; Universitas Gadjah Mada, Faculty of Medicine, Public Health, and Nursing, Center for Tropical Medicine), Mohammad Reza Masjedi (Pulmonary Medicine, Shahid Beheshti University of Medical Sciences, Iran, Islamic Republic; Cancer Control Research Center, Cancer Control Foundation, Iran University of Medical Sciences, Tehran, Iran; Tobacco Control Research Center (TCRC), Iranian Anti-Tobacco Association, Iran University of Medical Sciences, Tehran, Iran), Hashim Talib Hashim (University of Warith Al-anbiyaa, Colleges of Medicine, Karbala, Iraq), Peter Owiti (Stop TB Partnership/Wote Youth Development Projects, Kenya), Shaiirbek Sulaimanov (Kyrgyz-Russian Slavic University and Kyrgyz State Medical Academy, Kyrgyz Republic), Lawrence Oyewusi (Partners In Health, Lesotho), Boshra Abusahmin (National Centre for Disease Control, Libya), Mohamed Hadi Mohamed Abdelhamid (National Center for Disease Control (NCDC), Biotechnology Research Center (BTRC), Tripoli-Libya), Felix Mkandawire (Blantyre Malaria Project, Malawi), Ee Ming Khoo (Department of Primary Care Medicine, Faculty of Medicine, Universiti Malaya; International Primary Care Respiratory Group, Malaysia), Ousmane Ibrahim Diabate (Bamako, Mali), Adrian Rendon (CIPTIR, Hospital Universitario 'Dr Jose Eleuterio Gonzalez', UANL, Mexico), Berenice Soto-Moncivais (CIPTIR, Hospital Universitario 'Dr Jose Eleuterio Gonzalez', UANL, Mexico), Bolyskhan Baigabyl (Tuberculosis Clinic, National Center for Communicable Diseases, Mongolia), Celso Khosa (Instituto Nacional de Saúde-Centro de Investigação e Treino em Saúde da Polana Caniço (CISPOC), Marracuene, Mozambique), Cynthia Silva (Instituto Nacional de Saúde-Centro de Investigação e Treino em Saúde da Polana Caniço (CISPOC), Marracuene, Mozambique), Rajan Paudel (Birat Nepal Medical Trust, Nepal), Alberto Piubello (Damien Foundation, Niamey, Niger), Kadri Sani (Centre Hospitalier Régional, Niamey, Niger), Temitope Fapohunda (Lagos State University Teaching Hospital, Nigeria), Olayinka Adeyeye (Lagos State University, College of Medicine, Nigeria), Valentina Cvejoska Cholakovska (University Children's Clinic, Faculty of Medicine, Skopje, Ss Cyril and Methodius University of Skopje, North Macedonia), Ghulam Mustafa (College of Medicine Shaqra University Riyadh, Nishtar Medical University, Multan, Pakistan), Javier Cabrera-Sanchez (Facultad de Medicina, Universidad Peruana Cayetano Heredia, Lima, Peru), Diana Deleanu (University of Medicine & Pharmacy Iuliu Hatieganu, Romania), Jean Pierre Sibomana (Butare University Teaching Hospital, Rwanda), Momar Mbodji (Dakar, Senegal), Vesna Vekovic (Children's Hospital for Lung Diseases and TB, University Hospital Dr Dragisa Misovic, Belgrade, Serbia), Zorica Zivkovic (Children's Hospital for Lung Diseases and TB, University Hospital Dr Dragisa Misovic, Belgrade, Serbia; Faculty of Pharmacy in Novi Sad, University Business Academy Novi Sad, Serbia), Osman Muhyadin Abdulle (Forlanini Hospital, National Tuberculosis Program and Somaville University, Mogadishu, Somalia), Babiker Adam (M-Pharma, South Sudan), Sisira Siribaddana (Rajarata University of Sri Lanka, Teaching Hospital Anuradhapura, Sri Lanka), Rana Ahmed (The Epidemiological Laboratory, Khartoum, Sudan), Mahdia Elhadi (University of Hail, Sudan), Mohamed Elmustafa (University of Gezira; Wad Medani College of Medical Sciences and Technology, Sudan), Yousser Mohammad (Tishreen University, Latakia; Al Sham Private University, Damascus, Syria, Syrian Arab Republic), Stellah Mpagama (Kibong'oto Infectious Diseases Hospital, Tanzania), Bibie Said (Kibong'oto Infectious Diseases Hospital, Tanzania), Mongkol Lao-Araya (Chiang Mai University Hospital, Faculty of Medicine, Chiang Mai University, Thailand), Benilda Trias de Gula (Saint Paul Clinic of the Sisters of St Paul of Chartres Congregation, Timor-Leste), Agnes Hamzaoui (Hopital A Mami, Ariana and Medicine School, Tunis, Tunisia), Kübra Tunçel (University of Gazi, Turkiye), Islam Sangac (Turkiye), Tuğçe Tayyar (Lavanta Pharmacy, Turkiye), Aygün Gürgöze (Polatlı Can Hospital, Turkiye), Rebecca Nantanda (Makerere University Ung Institute, College of Health Sciences, Makerere University, Uganda), Maria Montes de Oca (Universidad Central de Venezuela, Centro Medico de Caracas, Venezuela), Juan Catari (Centro Medico de Caracas, Venezuela), Tran Thien Quan Vu (University of Medicine and Pharmacy at Ho Chi Minh City, Vietnam), Mohammed Mohammed (Al Taaon Pharmacy, Yemen, Rep), Ruba Khaled (Yemen, Rep), Weiam Hussein (Yemen, Rep), Charles Mataya Mphuka (Livingstone Central Hospital, Zambia), Terrence Rudado Musekiwa (Chimhanda District Hospital, Zimbabwe).

    • Contributors MS and KM devised the study. OBO, SJ, DMGH, RN, JM and CP provided input on the protocol. All Chronic Respiratory Diseases Medicines Survey Investigators contributed to data collection. MS completed the analysis with KM, and both assessed and verified the data. MS wrote a first draft, with input from KM, OBO, SJ, DMGH, RN, BWA, JM and CP. All investigators were invited to comment on a second draft. All had full access to all the data in the study and had final responsibility to submit for publication.

    • Funding MS was funded by a Wellcome Trust Clinical PhD Fellowship (Grant No 203919/Z/16/Z). JM was funded by a Medical Research Council Skills Development Fellowship (MR/S02042X/1).

    • Disclaimer The authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy or views of the Wellcome Trust or MRC.

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    • Competing interests KM reports advisory board fees from AstraZeneca and GlaxoSmithKline.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.