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Moving Mountains: The Evolution of USAID's Malaria Control Program  - Roger Bate, Richard Tren, Philip Coticelli
The President's Malaria Initiative and USAID both made progress in the fight against malaria in 2006. The true test of success moving forward will be how well African countries can sustain and build upon donor success.

World Bank Matrix (Malaria Booster Program) - Analysis for Africa Fighting Malaria  - Dr Roger Bate
The World Bank recently issued a malaria matrix, detailing spending on malaria control along with outcomes and targets. Roger Bate undertook an analysis of this matrix for AFM which critically analyzes the quality of the data and the logic of the World Bank undetaking this project.

Report on East and Southern Africa Malaria Conference  - Jasson Urbach
AFM's Jasson Urbach reports back on the recent East and Southern Africa Malaria Control Conference, held in Harare, Zimbabwe between 14 and 18 August.

DDT and neurodevelopment: results inconclusive to effect policy change  - Ameena E Goga
This reponse to Eskenazi et al.'s recent study on the link between DDT and childhood neurodevelopment argues that more data is needed to properly consider the implications for malaria control.

Tariffs, Corruption and Other Impediments to Medicinal Access in Developing Countries. Field Evidence  - Roger Bate, Lorraine Mooney, Richard Tren, Kathryn Boateng
AEI and AFM collaborate on a study investigating the incidcence of corruption and import tariffs on medicines and the impact on access to medicines in poor countries.

Government-Controlled Research and Development - A recipe for disaster  - Richard Tren & Roger Bate
The proposed research and development (R&D;) treaty being discussed at the World Health Assembly during the week of May 22 could end up harming those it aims to assist. Public-private partnerships, which are already delivering drugs and treatments and showing promise in vaccine development, offer a far better model to address diseases. Greater state and bureaucratic control of R&D; will not deliver results, especially given the need to deploy unique private-sector testing and development facilities. A range of market-friendly proposals to encourage research is likely to deliver practical solutions.


The World Bank: false financial and statistical accounts and medical malpractice in malaria treatment  - Amir Attaran et al
Amir Attaran & malaria experts & health policy commentators, including Africa Fighting Malaria's Roger Bate criticise the World Bank's failures in malaria control.

Still Taxed to Death: An Analysis of Taxes and Tariffs on Medicines, Vaccines and Medical Devices  - Roger Bate, Richard Tren & Jasson Urbach
Bate, Tren & Urbach update their working paper on taxes and tariffs on medicines and medical devices - published by the AEI-Brookings Joint Centre.

The WTO and Access to Essential Medicines: Recent Agreements , New Assignments  - Dr Roger Bate & Richard Tren
Roger Bate and Richard Tren discuss the recent WTO agreement on TRIPS and public health and recommend that the WTO now turn its attention towards removing import tariffs on medicines and medical devices, which have been shown to reduce access to medicines and medical care.

Brazil's AIDS Program - A Costly Success  - Richard Tren & Roger Bate
Richard Tren & Roger Bate comment on Brazil's AIDS Treatment program which has achieved some notable successes, but potentially reduces research into new AIDS medicines and could result in large long term costs down the line.

AFM testimony to the US Senate Committee on Environment & Public Works  - Roger Bate & Richard Tren
Download the testimony given by AFM's Roger Bate and Richard Tren to the US Senate's Committee on Environment and Public Works. The hearing, chaired by Sen. Inhofe (R, OK) was set up to look at the role of science and environmental policy - what better case study than DDT?

An Immesurable Crisis? A Criticism of the Millennium Development Goals and Why They Cannot Be Measured  - Prof. Amir Attaran
Prof. Amir Attaran evaluates the Millennium Development Goals and criticises them for being unmeasurable and therefore largely meaningless. He also criticises the UN for failing to discuss the measurement of these goals at the September 2005 UN meeting on the MDGs.

State in Fear - Zimbabwe's Tragedy is Africa's Shame  - Archbishop Pius Ncube, Dr Roger Bate & Richard Tren
Catholic Archbishop of Bulawayo Pius Ncube, Dr Roger Bate and Richard Tren report on the horrific abuses of human rights by Mugabe's police and military. The authors call on the G8 leaders to exert pressure on African leaders, such as President Mbeki, to condemn Mugabe's regime and support the return of peace and democracy in Zimbabwe.

AFM's Comment on the WHA Malaria Resolution  - AFM
The World Health Assembly recently passed a resolution on malaria control. The WHO and UNICEF also recently published their World Malaria Report. AFM comments here on some aspects of the resolution and report.

Senate Hearings on USAID  -
The Senate Hearings on USAID's involvement in malaria control led to significant challenges to the agency's activities. Download the testimonies from USAID, Senator Sam Brownback, Professor Amir Attaran and AFM's Dr Roger Bate here.

Eliminate Neglected Diseases Act of 2005  -
Senator Sam Brownback's Eliminate Neglected Diseases Act of 2005 has been dropped in the US Senate. Read the Act and supporting documents here.

Taxed to Death  - Roger Bate, Richard Tren and Jasson Urbach
AFM publishes a working paper on the degree to which import tariffs, taxes and bureaucratic procedures block access to essential medicines in poor countries. See the latest version of this ongoing study here.

Despotism & Disease  - Richard Tren & Roger Bate
Africa Fighting Malaria report on the destruction of the Zimbabwean healthcare sector and the probable impacts on the entire region. Download the pdf version of this report here.

Ugandan Study Highlights Best Drug Combinations for Treating Malaria in Africa  - The Lancet
Results of a randomised trial from Uganda in this week’s issue of THE LANCET suggest that the drug combination of amodiaquine and sulfadoxine-pyrimethamine might offer the optimal treatment for malaria in terms of efficacy and cost-effectiveness in this region. The study also shows that the drug combination of chloroquine and sulfadoxine-pyrimethamine—the recommended first-line treatment in Uganda—is far less effective than other drug combinations.

Climate Change and Malaria  - Indur Goklany - with response from Sir David King
Indur Goklany offers some fascinating insights into climate change, malaria, poverty and development. Sir David King, the UK Government's chief scientific adviser gives a predicable response.

The Real Obstacles to Sound Treatment of AIDS in Poor Countries  - Roger Bate & Richard Tren
Writing for the American Enterprise Institute's Health Policy Outlook, Bate and Tren explore some of the reasons for low drug access in poor countries. Despite promises of cheap or free antiretroviral drugs, Bate and Tren argue that access to treatment in poor countries is abysmally low because of a lack of infrastructure, political indifference, excessive bureaucracy and taxes and tariffs.

South Africa's War Against Malaria - Lessons for the Developing World  - Richard Tren & Roger Bate
The Cato Institute published Richard Tren and Roger Bate's analysis of South Africa's recent history with malaria control. They argue that its policy on DDT use and Artemesinin based combination therapy provide excellent examples for other malarial countries.

SA's Leading Malaria Researchers Support DDT Use  -
South Africa’s leading malaria control experts, researchers and doctors support and endorse the use of the insecticide DDT to control malaria. Their statement is released in light of recent claims that DDT is harmful to human health and should be removed from South Africa’s malaria control programme.

South African Malaria Data  - SA Dept of Health
November 2003 - the malaria statistics show that malaria is still well under control in South Africa. A recent epidemic in the Limpopo Province was primarily caused by late spraying and poor case management.

South Africa Malaria Data  - SA Dept of Health
The latest data on malaria cases and deaths from South Africa show that the country's policy of indoor residual spraying with DDT (among other insecticides) and the use of artemesinin based combination therapy is working. KwaZulu Natal, traditionally the province with the worst malaria and the centre of the recent epidemic has only recorded 1 malaria death this year!

South Africa Malaria Statistics  - Dept of Health
The 11th Dept of Health Malaria Update shows the latest number of confirmed cases and deaths from malaria in the three malarial provinces of South Africa.

Saving Lives Today and Tomorrow  - Dr. Roger Bate
This paper analyses trends in drug development using data from the drug industry association, the Pharmaceutical Research and Manufacturers of America (PhRMA). Worryingly, the findings suggest that far fewer AIDS drugs are in development compared to several years ago, and at a time when drug development for other communicable diseases is increasing. There are several probable explanations for this phenomenon, but the least benign is the likelihood that continual pressure group and media attacks on the industry over pricing of drugs in Africa has reduced incentives for development of new AIDS medicines

South African Malaria Update  - SA Dept of Health
The latest malaria update from the Directorate of Communicable Diseases.

http://medicine.plosjournals.org/perlserv?request=get-document&doi=10.1371/journal.pmed.0030197

PLos Medicine: Public Library of Sciences

Volume 3 | Issue 6 | JUNE 2006

Manslaughter by Fake Artesunate in Asia - Will Africa Be Next?

Paul N. Newton*, Rose McGready, Facundo Fernandez, Michael D. Green, Manuela Sunjio, Carinne Bruneton, Souly Phanouvong, Pascal Millet, Christopher J. M. Whitty, Ambrose O. Talisuna, Stephane Proux, Eva Maria Christophel, Grace Malenga, Pratap Singhasivanon, Kalifa Bojang, Harparkash Kaur, Kevin Palmer, Nicholas P. J. Day, Brian M. Greenwood, François Nosten, Nicholas J. White

P. N. Newton, R. McGready, S. Proux, N. P. J. Day, F. Nosten, and N. J. White are at the Centre for Clinical Vaccinology and Tropical Medicine, University of Oxford, Churchill Hospital, Oxford, United Kingdom. P. N. Newton, N. P. J. Day, and N. J. White are at the Wellcome Trust-Mahosot Hospital-Oxford Tropical Medicine Research Collaboration, Mahosot Hospital, Vientiane, Lao PDR. R. McGready, S. Proux, and F. Nosten are at the Shoklo Malaria Research Unit, Mae Sot, Tak Province, Thailand. R. McGready, S. Proux, P. Singhasivanon, N. P. J. Day, F. Nosten, and N. J. White are at the Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand. F. Fernandez is at the School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, Georgia, United States of America. M. D. Green is at the Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America. M. Sunjio and P. Millet are at EA3677 Bases Thérapeutiques des Inflammations et des Infections, Université Victor Segalen, Bordeaux, France. C. Bruneton is at Réseau Médicaments et Développement, Paris, France. S. Phanouvong is at the Drug Quality and Information Program, Global Assistance Initiatives, United States Pharmacopeia, Rockville, Maryland, United States of America. C. J. M. Whitty, H. Kaur, and B. M. Greenwood are at the Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, University of London, London, United Kingdom. A. O. Talisuna is at the East African Network for Monitoring Antimalarial Treatment, and Ministry of Health, Uganda. E. M. Christophel and K. Palmer are at the Western Pacific Regional Office of the World Health Organization, Manila, Philippines. G. Malenga is at the Malaria Alert Centre, Bantyre, Malawi. K. Bojang is at the MRC Laboratories, Fajara, Banjul, The Gambia

Funding: P. Newton, R. McGready, S. Proux, N. Day, F. Nosten, and N. White are supported by the Wellcome Trust of Great Britain. C. Whitty, H. Kaur, and B. Greenwood are supported by the Bill and Melinda Gates Foundation through the Gates Malaria Partnership. The authors received no specific funding to write this article.

Competing Interests: The authors declare that they have no competing interests. The authors' funding bodies had no role in the preparation of this article.

Published: June 13, 2006

DOI: 10.1371/journal.pmed.0030197

Copyright: © 2006 Newton et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abbreviations: ACT, artemisinin derivative-based combination therapy

Citation: Newton PN, McGready R, Fernandez F, Green MD, Sunjio M, et al. (2006) Manslaughter by Fake Artesunate in Asia-Will Africa Be Next? PLoS Med 3(6): e197

* To whom correspondence should be addressed: E-mail: paul@tropmedres.ac


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Falciparum malaria kills, and it particularly kills the rural poor. Artemisinin derivatives, such as artesunate, are a vital component of Plasmodium falciparum malaria treatment and control in the face of globally increasing antimalarial drug resistance. Since 1998 a worsening epidemic of sophisticated counterfeit "artesunate" tablets (containing no artesunate) has plagued mainland Southeast Asia (see Figure S1). In some countries, most of the available artesunate is fake [1-5].

Artemisinin derivatives are remarkably rapid in their antimalarial effects, and they are very well tolerated. So where these medicines are available, they are sought after. But as they are relatively expensive, a demand is created for cheaper versions amongst the poorest and most vulnerable people, upon whom the counterfeiters have preyed-with fatal results.

Documented Death due to Fake Artesunate
The death of patients with untreated falciparum malaria, as a result of unwittingly taking fake artesunate, is hidden in the inadequately documented mortality statistics of the relatively voiceless rural poor. But there is no doubt that such deaths occur, and they are probably common.

In February 2005, a 23-year-old man presented with fever to a rural hospital in eastern Burma where he was diagnosed as having uncomplicated hyperparasitaemic falciparum malaria by microscopy (4.2% infected red blood cells). He was treated with oral artesunate, labelled as made by Guilin Pharmaceutical (Guangxi, People's Republic of China), 4 mg/kg once a day, the treatment of choice in this area. Since artemisinin derivatives have been used in this area, not one of 600 patients prospectively studied with 4% parasitaemia has died [6]. However, on the third night the young Burmese man became unconscious and was transferred to another hospital where he was found to be in a coma (Glasgow Coma Score = 3/15), with renal failure and a higher parasitaemia ( 5.5% infected red blood cells). He was perfused with intravenous fluids and received an injection of intravenous artesunate (2.4 mg/kg) and transferred to a third hospital where he died within 12 hours of arrival from cerebral malaria.

The original hospital sent the artesunate used to treat the patient for analysis by the Fast Red dye test [7]. We found that the artesunate was counterfeit. Based on the appearance of the counterfeit hologram affixed to the blister pack, it was identified as a Type 9 counterfeit artesunate (see Figure S1). Accurate mass measurements by direct time-of-flight mass spectrometry [8] revealed that the main active ingredient in this "drug" was paracetamol (acetaminophen), but that artesunate was also present in the tablet [9]. Quantification using high-performance liquid chromatography determined that the artesunate content was 10 mg per tablet, instead of the 50 mg of artesunate present in the genuine product [9].

The hospital where he was originally treated had, in good faith, recently purchased a large quantity of artesunate tablets. They were dismayed to learn from this death that their entire stock was fake. The village committee, which now had a clear idea of what was responsible for the man's death, was so angered by this avoidable death that they collected all the artesunate, fake and genuine, that they could find in local shops and destroyed it on a public bonfire in front of the whole village, to stress the lethal dangers of fake antimalarials.

The Epidemic of Counterfeit Artesunate in Southeast Asia
Counterfeit artesunate continues to circulate on a vast scale in mainland Southeast Asia, where between 38% and 52% of "artesunate" blister packs sampled contain no active ingredient [1-5]. So far, only the Guilin Pharmaceutical brand of artesunate has been counterfeited. We make no apology for the use of the term manslaughter to describe this criminal lethal trade. Indeed, some might call it murder. Somewhere, people are directing a highly technical and sophisticated criminal trade. They are making tablets out of starch, chalk, and a variety of wrong active ingredients, such as erythromycin [9,10], for a life-threatening disease that particularly affects the poor and underprivileged. The criminals are making these fakes in the full knowledge that their ineffective product might kill people who would otherwise survive their malaria infection.

There are now at least 12 different types of fake artesunate, classified by the sophisticated counterfeit holograms that are affixed to the blister packs (see Figure S1). Evidence suggests that production is on an industrial scale and from multiple sources; 100,000 counterfeit artesunate tablets were purchased from one large pharmacy [2].

This epidemic of a counterfeit, vital, life-saving medicine has received little practical attention over the last eight years, in comparison with the considerable efforts in other aspects of malaria control [3,11]. In addition to unnecessary loss of life for profit, it has led to a loss of confidence in these very effective medicines and given rise to false reports of artemisinin resistance [1,12]. Much more needs to be done in Asia to combat this scourge.

The Risk to Western Travellers
This criminal activity is unlikely to remain a local difficulty, and there are serious implications from this major public health problem for the wider world beyond Asia that deserve attention. In the industrialised North, with carefully regulated trade, the implications are limited. However, especially as the artemisinin derivatives have a natural plant origin, tourists commonly buy them in the tropics as a standby treatment [13]. Indeed, Web sites encourage this practice [14], which is likely to be compounded by the availability of artemisinin derivatives on the Internet [15]. It is inevitable that counterfeit artesunate will seep into this trade.

We suggest that travel clinics should warn those going to the tropics of the potential dangers of buying such drugs. Unfortunately, in our discriminatory world, the unnecessary death of a tourist, journalist, or of a diplomat or military personnel, from a wealthy, influential country after self-medicating with fake artesunate, may be required to trigger the political will required to eradicate this lethal trade.

Will Africa Be Next?
Of far greater concern is that counterfeits may follow in the wake of the genuine artesunate that is increasingly being imported for use in sub-Saharan Africa, where the burden of malaria is greatest. Since 2001, the World Health Organisation has recommended that malaria-endemic African countries should consider changing to artemisinin derivative- based combination therapy (ACT) as first-line malaria treatment. In the past two years, most countries in Africa (34 in 2004) have made this change [16]. Implementing this new policy will not be easy because of the high cost of ACTs and a temporary shortage of the plant raw material. It is estimated that 130 million courses of ACT will be used in Africa in 2006 [16]. High cost and shortage of ACT provide a favourable situation for the spread of fake artemisinins that could put the lives of thousands of African children at risk. There is already a thriving fake antimalarial drug industry in Africa [17], suggesting that it is highly likely that counterfeit artesunate or ACTs will follow in the wake of the genuine products, and in bulk.

Counterfeit dihydroartemisinin (60 mg per tablet; Cotexcin) was reported from Tanzania in 2001 [18], labelled as made by Beijing COTEC New Technology Corp, and containing no dihydroartemisinin or other active drug when analysed by thin layer chromatography and high-performance liquid chromatography (Figure 1, collection and analysis of the sample by MS, CB, and PM). In 2005, counterfeit artesunate tablets, mimicking Arsumax (50 mg per tablet; Sanofi Synthelabo, Bridgewater, New Jersey, United States) were found in Cameroon (Figure 2, collection and analysis of the sample by MS, CB, and PM). These were labelled as Arsuman manufactured by Sanofi Synthelabo, who confirmed that the packaging was counterfeit. On high-performance liquid chromatography analysis, these tablets did contain 50 mg of artesunate (MS, CB, PM), and this counterfeit is a look-alike copy of the genuine product. That at least two different counterfeit artemisinin derivatives have already been distributed in Africa is of considerable concern. Because of inadequate systems for the monitoring of the quality of antimalarial medicines, and because few have looked for it, counterfeit artesunate may already be widespread.


Figure 1. Genuine (Left) and Counterfeit (Right) Cotexcin (Dihydroartemisinin) from Tanzania (Photograph by Manuela Sunjio)

Figure 2. Genuine (Right) and Counterfeit (Left) Arsumax (Artesunate) from Cameroon (Photograph by Manuela Sunjio)
Note that the genuine Arsumax bears a hologram from Guilin Pharmaceutical, which manufactures the tablets (see Figure S1).

It is likely that, initially, most ACTs in Africa will be provided through the public health system where it should be relatively easy to control quality by purchasing only from established companies or from an international purchasing facility and by providing strong support to national quality control laboratories. However, the possibility of corruption within the national purchasing process cannot be excluded, as the potential financial gains for those involved could be very high.

In many parts of Africa, most patients with uncomplicated malaria obtain treatment from the private sector. Provision of free, or heavily subsidised, highly effective ACTs through public health facilities may reduce this proportion. However, it is likely that for the foreseeable future a substantial proportion of antimalarials used in Africa will be obtained through the private sector and it is here that the danger from fake artemisinins is greatest. Official promotional campaigns are likely to create immense demand for ACTs through the private system even though many potential users will struggle to meet their cost. In such a situation, introduction of a relatively inexpensive fake ACT product could lead to widespread usage of the fake drug with disastrous consequences.

Preventing an Epidemic of Fake Artesunate in Africa
How might the spread of fake artesunate be prevented? Control of medicine importation is a first barrier of defence, but this is difficult to maintain and antimalarials are readily shipped across porous frontiers. There are at least 11 different brands of oral artesunate available in sub-Saharan Africa, including the genuine Guilin Pharmaceutical product. One of the authors was recently offered seven different artemisinin derivative brands in one small-town West African pharmacy-it is unlikely that all of these had been imported through official channels.

A second more radical option is to ensure that ACTs provided through the private sector are relatively inexpensive and locally affordable so that there is no financial advantage to looking elsewhere and thereby unwittingly purchasing a fake. This would require some form of central subsidy, as recently suggested in an Institute of Medicine (Washington D. C., United States) report [19]. This recommendation was made primarily to increase access to ACTs and to discourage monotherapy with artemisinins or the partner medicine (the co-drug in ACT) and thus to protect the ACT from the emergence of resistant parasites. Such an approach would have the additional advantage of discouraging the use of fake artemisinin-based medicines, as the counterfeit manufacturers would have little margin to make a profit. We strongly suggest that African countries and health organisations support such strategies to try to prevent counterfeit artemisinins from infecting Africa, to establish effective systems to carefully monitor their antimalarial drug supply, and to prepare to counter a problem that, as is evident from Asia, is very difficult to eradicate once established.

Of global concern for the future of malaria control, some counterfeit artesunate samples (Types 4, 10, and 11) recently collected in eastern Burma do contain small subtherapeutic quantities of artesunate (3.5-12.1 mg/tablet [9]). P. falciparum parasites with stable in vivo resistance to the artemisinin derivatives have not yet been described from the wild, but parasites with reduced in vitro sensitivity to artemether have recently been reported [20]. The in vivo exposure of parasites to low concentrations of artesunate from fake products will greatly increase the risk of the selection and spread of artemisinin resistant parasites, leading to the catastrophic loss of these essential medicines and an entirely avoidable failure of malaria control. We cannot afford to lose these drugs, as we have lost chloroquine and sulphadoxine-pyrimethamine-most current combinations depend on ACTs. In addition, the presence of small quantities of artesunate in tablets may mean that the Fast Red dye test [7], widely used for screening the quality of artesunate tablets, may give false positive results depending on how much artesunate is present in these fakes.

Conclusion
Fake artesunate could compromise the hope that ACT therapy offers for malaria control in Africa and Asia. Fakes containing subtherapeutic amounts of artesunate could also result in the emergence and spread of resistance to the artemisinin drugs, shortening the useful life of these vital medicines. But this tragedy is avoidable, if there is sufficient political will. As global efforts to control malaria rely heavily on these drugs, these issues deserve overdue, urgent action to prevent a public health disaster in the malarious world.

Supporting Information
Figure S1. Fake Artesunate Warning Sheet Number 4, April 2006
At least 12 different types of fake artesunate are being sold in mainland Southeast Asia. This warning sheet gives some key features to aid identification of these fakes.

(1.1 MB PDF).

Acknowledgments
We are very grateful to anonymous colleagues for their considerable help, to all who have helped with the collection of artesunate samples, and to Hubert Berennes and Michel Strobel.

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