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A Case of Plasmodium Falciparum Malaria Presentation

Editor(s): Naveed, Khan.

From the Lincoln Medical and Mental Health Center, New York, New York, USA.

Correspondence: Osman Nawazish Salaria, Lincoln Medical Center, New York, New York USA (email: [email protected] ).

Abbreviations: BPb = lood pressure, bpm = beats per minute, BUNb = lood urea nitrogen, CDC = Center for Disease Control, cm = centimeters, Creatc = reatinine, DOHMH = Department of Health and Mental Hygiene, ED = Emergency Department, Hb = hemoglobin, Hct = hematocrit, ICU = intensive care unit, IV = intravenous, IVP = intravenous push, Plt = platelet, WBC = white blood cell, WHO = World Health Organization, y/o = year old.

Methods: Ethical approval was not necessary for this study as the study was focused on the patient hospital course and did in no way alter or affect her treatment. Informed Consent was taken from the patient regarding the publishing of this case report and the patient accepted.

The authors have no conflicts of interest to disclose.

This is an open access article distributed under the Creative Commons Attribution License 4.0, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. http://creativecommons.org/licenses/by/4.0

Received April 20, 2015

Received in revised form July 11, 2015

Accepted July 27, 2015

New York City is a multicultural city where people of different ethnicities and backgrounds from all over the world live together. Of the different ethnicities, it is home to a large population of Western African immigrants. This case report is that of an elderly female of Western African descent presenting to Lincoln Hospitals Emergency Department with fevers and fatigue.

The patients travel history to Togo, along with her symptoms, resulted in a differential diagnosis which included Ebola as well as Malaria. New York City's Department of Health and Mental Hygiene was contacted for further clarification of presence of Ebola in Togo. The present case report is meant to educate about the presentation, hospital course, and differential diagnoses of a patient traveling from Western Africa with fever and chills.

INTRODUCTION

Malaria is a frequent parasitic infection prevalent in Africa. Around 300 million are infected annually in Africa by malaria and 1 to 2 million will die from the disease. 1 Of the 4 human parasitic species that have been identified, Plasmodium falciparum has been known to cause significant morbidity and mortality, particularly in children and pregnant women. 1 Strategies to counteract malaria incidence, such as community health workers outreach and insecticide treated nets have been instituted in recent years; however, their effect has not been of much significance. 2

Ebola virus disease has caused much concern with its global rise in incidence and prevalence recently. The current epidemic which has centered mainly in Western African nations of Guinea, Sierra Leone, and Liberia has now spread outside of borders of Africa to involve the United States. 3 Much of the presenting symptoms and signs of the disease mimic other diseases such as typhoid fever and malaria. 3,4

There is much overlap between presentations of both P. falciparum malaria and Ebola virus disease. Without confirmatory blood tests searching for malaria parasites or viral RNA and viral antibodies a diagnosis is very difficult to achieve.

CASE REPORT

A 67 y/o (year old) female from Western Africa initially presented to the Emergency Department (ED) complaining of fatigue and subjective fevers for the past 2 days. Patient complained that her fevers were associated with headaches, but not chills, rigors, or chest pain. Index of suspicion for malaria was high as patient had recently traveled from an endemic region. Patients travel history to Western Africa and the presenting symptoms also made us consider a possibility of Ebola virus disease.

Past medical history included diabetes, hypertension, and a history of recent travel to her home country of Togo for 5 months. Patient had returned 5 days ago from her travel and started to develop symptoms of fevers and fatigue. Patient denied any immunizations received before traveling. Past surgical history included a left breast mastectomy done back in France 1987. Medication history included Amlodipine, Aspirin, Calcium Carbonate, Synthroid, Pioglitazone, Humalog, Glucovance, Crestor, Januvia, and Lisinopril. After initial presentation to the ED for 2 days of fevers and fatigue, she was accepted by Medicine and transferred to the general medical floors. The patient had a blood pressure of 123/55, pulse of 86 beats per minute (bpm), Temperature of 98.5 °F, and respiratory rate of 16 at the time of admission. Physical examination did not disclose any specific abnormalities.

Labs including complete blood count, chemistry, liver function tests, malaria peripheral smears, and reitculocyte level were withdrawn from the patient. Patient had white blood cell (WBC) count of 12.6, Hb (hemoglobin) 10.7, Hct (hematocrit) 30.6, Plt (platelet) 80, BUN (blood urea nitrogen) 12, Creat (creatinine) 0.3, and blood glucose of 291 consistent with diabetes. Blood smears were positive for P. falciparum malaria at 9.6% and reticulocyte count was reported at 3.2%. New York City's Department of Health and Mental Hygiene (DOHMH), was contacted and Ebola was not considered to be in Togo, most likely diagnosis was malaria from chloroquine resistant region. Patient was started on quinine 648 mg and doxycycline 100 mg, intravenous (IV) fluids, Lantus 21 U, Lispro 7 U, and was monitored in telemetry unit of medicine (Figures 1–3).

Attention was drawn to the patient at 4:45 AM on her 3rd hospital course day after becoming suddenly dyspneic. Patient denied any chest pain but upon pulmonary examination bilateral coarse crackles were heard up to mid lung level. Patient received 60 mg intravenous push (IVP) Lasix and sublingual nitroglycerin. She continued to be dyspneic and was given additional 40 mg IV Lasix and 4 mg Morphine IV were given. Bi-continuous positive airway pressure was started but patient did not tolerate well and decision was made to intubate the patient for acute hypoxemic respiratory failure. Patient was transferred to the medical intensive care unit (ICU) for further care.

Chest X-ray in the medical ICU revealed bilateral alveolar infiltrates; patient was started on Cefepime 2 g IV. Presumption was made that patient had Acute Respiratory Distress Syndrome secondary to sepsis from an unknown source of infection, but possibly from Falciparum Malaria. Abdominal ultrasound showed tiny echogenic foci within the gallbladder, prominent liver measuring 18.7 cm, and a dilated common bile duct measuring 8.2 mm. Choledocholithiasis was questioned although not directly visualized. Decision was made to monitor liver enzymes and if worsening of abdominal status cholecystostomy tube could be placed.

Patient remained in the medical ICU where she was daily monitored. Vital signs monitoring showed daily fever spikes of 101 to 103 °F 2 to 3 times per day. Liver enzymes were down trending after week 1, repeat right upper quadrant ultrasound was negative most probably from passage of a gallstone. On day 9 of hospital course patient was extubated and transferred to medical floors for continuation of care.

Patients of Western African descent presenting with symptoms of fevers and fatigue must be approached with precaution in present day circumstances. The Ebola virus disease outbreak has currently heightened healthcare professional's fears of contracting the virus by exposure to their patients. Furthermore, the impact of the Ebola virus disease in West Africa has left the local population vulnerable to other deadly diseases such as malaria. Control efforts for disease transmission and treatment of malaria have come to a halt. Anti-malaria medication, preventive insecticide bed nets are lying in warehouses far from the people which could benefit from them. International agencies such as the World Health Organization (WHO), US Agency for International Development supported and funded programs malaria control initiatives have virtually been shut down. 5 The similarities of the symptoms and signs of presentation of both diseases intimidates people from seeking treatment for fear of being infected with Ebola.

In face of all these difficulties, Ebola control efforts including government education programs partnered with WHO, travel measures has reduced the incidence significantly. Early identification of symptoms, isolation of contacts, and early monitoring and treatment has played a major role in limiting spread of infection of Ebola. This case report illustrates an example of how a patient with recent travel history to West Africa presenting with typical fevers, myalgias, and fatigue could be considered to have either or both diseases.

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• Am J Trop Med Hyg
• v.89(3); 2013 Sep 4

Case Report

Two cases of plasmodium falciparum malaria in the netherlands without recent travel to a malaria-endemic country.

Recently, two patients of African origin were given a diagnosis of Plasmodium falciparum malaria without recent travel to a malaria-endemic country. This observation highlights the importance for clinicians to consider tropical malaria in patients with fever. Possible transmission routes of P. falciparum to these patients will be discussed. From a public health perspective, international collaboration is crucial when potential cases of European autochthonous P. falciparum malaria in Europe re considered.

Plasmodium falciparum malaria is an important cause of morbidity and mortality worldwide. 1 It is not endemic to Europe, and reported cases in Europe are almost exclusively in travelers returning from malaria-endemic areas. 2 Imported infections with P. falciparum ( P. falciparum malaria) account for most malaria-related morbidity and mortality in Europe. 3 The Netherlands was declared malaria free by the World Health Organization in 1970.

The incubation period of P. falciparum malaria is 12–14 days, but longer incubation periods can occur in semi-immune persons and persons taking ineffective malaria prophylaxis, but is typically less than one month. 4 , 5 Importantly, diagnosis of P. falciparum malaria may be missed or delayed in patients who have malaria years after leaving a malaria-endemic area or who do not report recent visits to malaria-endemic countries. 6 However, early detection of apparently non-imported cases of P. falciparum malaria in Europe is of major public health importance because it enables effective response activities to prevent outbreaks. We describe two patients who had not been in malaria-endemic areas for years, but had P. falciparum malaria shortly after returning from countries in southern Europe. Informed consent was obtained from the patients for publication of this report.

Case-Patient 1

A 23-year-old man from Liberia was seen at an emergency department in the Netherlands because of abdominal pain for three days and a fever of 40°C. Besides an episode of malaria in the past (before 2008), he had no medical history. His travel history indicated a visit to a malaria-endemic country, Liberia, in 2008. Nine days before admission to our hospital, he returned from a four-week holiday in Barcelona, Spain and Treviso, Italy, where he traveled by car. During his travel, he stayed with immigrants who recently returned from Africa, some of whom were sick and had fevers. The patient reported that in both places the living conditions were poor, and many indoor insects, including mosquitoes, were present. No other risk factors for transmission of malaria (e.g., intravenous drug use, blood transfusion, surgical interventions, airport visit) were reported.

At a physical examination, he did not appear acutely ill. His blood pressure was 108/55 mm of Hg, his pulse rate was 84 beats/minute and his temperature was 40 °C. He had abdominal tenderness. There were no other abnormalities. Laboratory test results showed hemoglobin level of 8.3 mmol/L, a thrombocyte count of 56 × 10 9 /L, a leukocyte count of 4.5 × 10 9 cells/L and a normal differentiation pattern, a C-reactive protein level of 127 mg/L, and a lactate dehydrogenase level of 278 U/L. Surprisingly, examination of a peripheral blood smear showed P. falciparum- infected erythrocytes with a parasitemia index of 2.3%. A rapid immunographic test (Binax NOW Malaria Test; Binax, Portland, OR) result for P. falciparum was positive.

The patient was initially treated with intravenous quinine and improved after one day. After an initial increase of his parasitemia to 4.6% it decreased to < 0.1% after 3 days, after which he was treated with four tablets of atovaquone/proguanil a day for three days. He fully recovered and at follow-up visits at the outpatients department, no malaria parasites were seen on a thick blood smear. Although the patient denied making any recent visits to tropical areas, his blood count revealed 17 × 10 9 eosinophils/L and his feces contained Schistosoma mansoni eggs. He was then successfully treated with praziquantel.

Case-Patient 2

A 34-year-old woman from Sierra Leone was seen at an emergency department in the Netherlands because of periodic spiking fever that lasted for two weeks. Her medical history was unremarkable, except for uterine fibroids and an episode of malaria several years ago. She used no medications. Besides the fever, she had abdominal pain and arthralgia since that time. She noticed that her symptoms felt like malaria, which she experienced in the past in her home country. Her travel history showed that her last visit to a malaria-endemic country, Sierra Leone, was in 2003. In recent years, her travel was limited to Belgium and France. On the first day she experienced symptoms, she had returned from a four-week stay in the Bourgogne area in central France, where she spent time in an apartment block with family and friends. According to the patient, several persons who recently returned from Africa to the apartment block, came down with malaria-like symptoms in the same period. The patient also reported a one-day visit to Charles de Gaulle International Airport. No other risk factors for the recent infection (e.g., intravenous drug use, blood transfusion, surgical interventions) were reported.

At a physical examination, she did not appear sick or anemic. Her blood pressure was 150/90 mm of Hg, her pulse rate was 85 beats/minute and her temperature was 36°C. Peripheral oxygen saturation was 98% at room temperature, and her respiratory frequency was normal. Abdominal examination showed uterine fibroids, which were known to be present, but no hepatosplenomegaly. Several small wounds, possibly caused by insect bites, were seen around her ankles.

At laboratory test examination, the most striking findings were an anemia with an hemoglobin level of 7.1 mmol/L (11.4 g/dL), thrombocytopenia (80 × 10 9 cells/), and slight leukocytopenia (3.7 × 10 9 /L) and a normal differentiation. Lactate dehydrogenase (501 U/L) and C-reactive protein (109 mg/L) levels increased. A chest radiograph showed no abnormalities.

Despite absence of recent travel to malaria-endemic areas in her travel history, but given the patient's remark about her symptoms resembling malaria, microscopy of a thick blood smear and malaria antigen test (Binax NOW malaria test; Binax) were performed and showed an infection with P. falciparum with a parasitemia of 0.18% and gametocytes. She received a 3-day course of atovaquon/proguanil (4 tablets/day) and was sent home. She fully recovered and in follow-up visits at the outpatients department, no malaria parasites were seen on a thick blood smear.

We describe two residents of the Netherlands, both originating from Africa, who came to two hospitals in the Netherlands with P. falciparum infections. Thorough reviews of their travel histories did not show visits to a malaria-endemic area in recent years, but visits to different areas in Europe: Italy, Spain (patient 1), and France (patient 2). Other patients with a P. falciparum infection without a designated source have been reported in Germany. 7

These observations are important because of their relevance for public health and clinical practice. Regarding clinical practice, P. falciparum infections are rarely considered in the differential diagnosis of patients with fever returning from these parts of Europe. For clinicians in the Netherlands, malaria is a traveler's disease and often only considered when patients return from malaria-endemic (i.e., tropical) countries. A delay in the diagnosis and treatment of P. falciparum malaria can lead to increased morbidity and mortality. 8 Therefore, a thorough review of the travel history is important in establishing the origin of the infection.

Discrepancies between reported and actual travel history may occur, giving rise to uncertainties and unexplained symptoms, such as signs of schistosomiasis despite absence of recent travel to tropical areas in the travel history reported by case-patient 1. 9 There are no formal barriers against accessing emergency health care for anyone in the Netherlands. However, it is known from anecdotal evidence reported by clinicians that immigrants unjustly fear the existence of formal barriers, including payments and connections between immigrant regulations and health care and public health authorities. These barriers can potentially influence the reporting of their travel history, limiting thorough analysis of the transmission routes, including on-site entomologic investigations.

In accordance with the Public Health Act, both patients were reported to the Municipal Health Services and subsequently to the Dutch National Institute for Public Health and the Environment. Reporting of these patients in a short time interval without reported travel history to a malaria-endemic country was considered remarkable. European autochthonous malaria was considered as a diagnosis ( Table 1 ). The Dutch National Institute for Public Health and the Environment informed the French, Spanish and Italian Public Health Authorities in France, Spain, and Italy through the European selective exchange Early Warning and Response System.

Possible routes of Plasmodium falciparum transmission for the two case-patients described, the Netherlands

During the past few years, outbreaks of P. vivax malaria have occurred in parts of southeastern Europe, but P. falciparum malaria outbreaks have not been reported. 10 Historically, P. vivax in Europe has been transmitted predominantly by five Anopheles species. 11 However, these mosquito species have been shown to be incompetent for transmitting P. falciparum malaria. 12 The only two mosquito species in Europe known to be competent for transmitting P. falciparum are Anopheles algeriensis and An. plumbeus . 13

Theoretically, with the presence of P. falciparum -competent mosquito species, local malaria transmission is possible when gametocyte-carrying persons that are infected in malaria-endemic areas reside in Europe. 14 This hypothesis of local household transmission in France is supported by the fact that insect bite wounds on the lower extremities were reported by the second patient, whereas the indoor presence of mosquitoes, as well as other persons with malaria-like symptoms at the visiting location, were reported by both patients. However, no autochthonous transmission of P. falciparum has been reported in Italy, Spain, France, or any other country in Europe in 2012 ( http://data.euro.who.int/cisid/?TabID=303151 ). Unfortunately, neither patient was willing to reveal their exact locations of stay, making any follow-up in France, Italy, or Spain impossible.

Local transmission in the Netherlands was also considered but seems unlikely. If one considers that the duration between infection and development of gametocytes was at least 14 days, symptoms developed in both patients within 1 and 9 days, respectively, after returning from travel, and gametocytes in blood smears in relation to reported recent travel of the patients, these three factors probably exclude infection acquired in the Netherlands. Anopheles plumbeus is endemic in the Netherlands. However, in the current circumstances, the vector capacity is considered to be low. There are no indications of autochthonous transmission. 15

The latest reported cases of locally acquired tropical malaria in the Netherlands could be explained by airport malaria in patients staying near Schiphol Airport. 16 , 17 This so-called airport malaria could be another possible route of transmission in our patients. Mosquitoes can hide in freight or passengers area of the planes, or can be transported in the wheel bays and released when the bays open during the approach for landing. 18 – 21 Neither of the patients lived near an airport in the Netherlands, but airport malaria could have been a mode of infection for the second patient because she mentioned that she paid a one-day visit to Charles de Gaulle International Airport during her visit to France. Luggage malaria could also be a route of transmission because both patients visited friends who recently came from malaria-endemic countries. Mosquitoes could have been imported in their suitcases.

Plasmodium falciparum transmission by direct inoculation of infected blood is considered a route of transmission. However, neither of the two patients had received blood or undergone recent medical procedures before infection, reported use of intravenous drugs, or had scars at the physical examination. 22 – 24

Finally, late recrudescence or relapse has been described for different forms of malaria, mostly associated with P. malariae , P. vivax , 25 – 29 or P. ovale . 30 , 31 Interestingly, our patients were originally from malaria-endemic countries, but they reported that they had not returned to their countries of origin for four and nine years, respectively. Late recrudescence of tropical malaria has been described in immunocompromized patients or pregnant women, although these findings are extremely uncommon. 32 – 35

Several cases have been attributed to infected Anopheles spp. mosquitoes traveling in luggage or at least associated with pre-existing partial immunity from repeated prior exposures. 33 Late recrudescence caused by pregnancy or immunosuppression in our patients was considered unlikely.

In conclusion, we report two P. falciparum malaria patients without reported recent travel to a malaria-endemic area. Physicians should be aware of the possibility of P. falciparum infections in patients who have been in contact with travelers who recently returned from malaria-endemic area (luggage, airport, local transmission). Rapid communication between physicians and public health authorities in Europe is needed to effectively respond to signs of possible autochthonous transmission.

ACKNOWLEDGMENTS

We thank our colleagues in France, Italy, and Spain with whom we communicated through the Early Warning and Response System and our colleagues at the Municipal Health Service Utrecht and the Municipal Health Service Midden Nederland for their work and expertise. We also Dr. Marieta Braks (National Institute for Public Health and the Environment) for her contributions to the manuscript. Joop E. Arends and Jan Jelrik Oosterheert managed patients and wrote and edited the manuscript; Marleen M. Kraaij-Dirkzwager and Ewout B. Fanoy were responsible for possible outbreak investigation and edited the manuscript; Jan A. Kaan performed microbiologic diagnosis and edited the manuscript; Pieter-Jan Haas performed microbiologic diagnosis; Ernst-Jan Scholte and Laetitia M. Kortbeek performed vector analysis; and S. Sankatsing managed patients and edited the manuscript. The American Committee on Clinical Tropical Medicine and Travelers' Health (ACCTMTH) assisted with publication expenses.

Authors' addresses: Joop E. Arends, Jan Jelrik Oosterheert, and Pieter-Jan Haas, Department of Internal Medicine and Infectious Diseases and Department of Medical Microbiology, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, The Netherlands, E-mails: [email protected] , [email protected] , and [email protected] . Marleen M. Kraaij-Dirkzwager, Department of Infectious Diseases, National Institute for Public Health and the Environment, Bilthoven, The Netherlands, E-mail: [email protected] . Jan A. Kaan, Department of Medical Microbiology and Immunology, Diakonessenhuis Utrecht, Utrecht, The Netherlands, E-mail: ln.siuhkaid@naakj . Ewout B. Fanoy, Infectieziekten, Municipal Health, Midden-Nederland, Zeist, The Netherlands, E-mail: ln.nmdgg@yonafe . Ernst-Jan Scholte, Laboratory of Entomology, Wageningen University, Binnenhaven 7, Wageningen 6700 EH, The Netherlands, E-mail: [email protected] . Laetitia M. Kortbeek, Department of Diagnostic Laboratory for Infectious Diseases and Perinatal Screening, National Institute of Public Health and the Environment, Bilthoven 3720BA, The Netherlands, E-mail: [email protected] . Sanjay U. C. Sankatsing, Department of Internal Medicine and Infectious Diseases, Diakonessenhuis Utrecht, Utrecht, The Netherlands, E-mail: ln.siuhkaid@gnistaknass .

Pulmonology (previously Revista Portuguesa de Pneumologia) is the official journal of the Portuguese Society of Pulmonology (Sociedade Portuguesa de Pneumologia/SPP). The journal publishes 6 issues per year, mainly about respiratory system diseases in adults and clinical research. This work can range from peer-reviewed original articles to review articles, editorials, and opinion articles. The journal is printed in English, and is freely available in its web page as well as in Medline and other databases.

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• Palavras-chave
• Introduction
• Case report
• Discussion and conclusions

We report a clinical case of severe malaria, where the rate of initial parasitaemia by Plasmodium falciparum was 43 %.

Multiple organ dysfunction, including ARDS, forced admission in a close surveillance unit, with survival of the same.

A brief review of the subject is made, focusing on severity and general conduct, alerting and awareness for this entity, whose expression, among us, could take on increasing importance.

Apresenta-se o caso clínico de um doente regressado de Angola com malária grave, em que o índice de parasitémia inicial pelo P. falciparum era de 43 %.

Disfunção múltipla de orgãos, incluindo ARDS, implicaram o ingresso do doente numa unidade de alta vigilância, com sobrevivência do mesmo.

Faz-se uma breve revisão do assunto, com enfoque nos indicadores de gravidade e na conduta geral, alertando e sensibilizando para esta entidade, cuja expressão, entre nós, poderá vir a assumir importância crescente.

Malaria is caused by the protozoa Plasmodium , 1 with an intra and extra erythrocyte life cycle, and man is infected by the bite of the anopheles mosquito. There are four species responsible for human malaria: Plasmodium falciparum, P. vivax, P. ovale and P. malariae.

Most cases of imported malaria are caused by P. falciparum. It is characterized by fever, chills, intense sweating and headaches, that arise between the 9 th and 14 th days after bite. Incubation can last for months.

With postponed diagnosis erythrocyte parasitemia may reach critical values, massive hemolysis and multiorgan dysfunction resulting in death.

The pulmonary involvement with edema is a major complication. 2 More common in adults, is more severe in pregnant and non-immunized individuals. 3 The alveolar-capillary barrier suffers increased permeability and alveolar flooding, conditioning acute lung injury/acute respiratory distress syndrome (ARDS). 4

Man, 44 year old, black, born in Angola and resident in Portugal for 24 years, where he works in building construction.

Medical and surgical history irrelevant. Denies alcohol or smoking habits, illicit drug use or sexual risk contacts. He had returned from Angola two weeks ago from his first trip there, without taking any precaution.

He recurs to the emergency room with fever (40 ºC) and general malaise of a week duration, and watery stools since the last three days.

He presented with a reasonable general condition, dry mucous membranes and icteric sclerae. A hypotensive and tachycardic profile was noted, while being apyretic with good peripheral saturations on ambient air.

No obvious focus of infection was detected and the rest of the objective examination was irrelevant.

Initial laboratory parameters was as follow: hemoglobin 11.9 g/dL, WBC 7,200/μL, platelets 27,000/μL; normal ionogram and renal function, mild liver cytolysis without hyperbilirubinemia, LDH 693 U/L, C-reactive protein (CRP) 228.9 mg/dL. Positive thick smear for Plasmodium with 43 % of parasitemia ( Fig. 1 ).

Picture of the patient's peripheral blood smear showing a very high level of parasitemia with images of trophozoites and merozoites, as well as significant schizocytes. There were no gametocytes and therefore cannot be seen here.

Therapy was started with quinine sulfate and doxycycline.

Infection with hepatotropic virus, HIV I/II, intestinal parasites, urinary tract infection, bacterial gastroenteritis or bacteraemia was excluded. The chest radiograph shows no abnormality.

On the 3 rd hospital day (D3), the patient became more obtunded, pale, dehydrated, and more icteric with profuse sweating, fever, tachypnea and hemodynamic instability. On pulmonary auscultation there was new bilateral inspiratory crackles.

Hemoglobin fall to 6.8 g/dL accompanied by hyperbilirubinemia, LDH = 801 U/L, haptoglobin mg/dL, thrombocytopenia (37,000/μL), creatinine 1.7 mg/dL and mild hyponatremia. The CRP remained high and procalcitonin reached 42.6 mg/dL. Plasmodium on direct examination was negative. The characterization of the agent trough the BinaxNOW® test showed a single antigen band for P. falciparum.

The patient was admitted to a High-Dependency Unit (HDU), with multiple dysfunctions, including cardiovascular, hematological, renal, hepatic and respiratory systems (PaO 2 /FiO 2 = 129) with criteria for ARDS ( Fig. 2 ). After attempts was made to exclude secondary septic complications, to the general support measures, which included liberal fluids infusion and transfusion of packed red blood cells, an empiric antimicrobial coverage with linezolid plus piperacillin/tazobactam was instituted.

Chest anteroposterior teleradiography of the 5 th day, on the left, and of the 10 th day of hospitalization, on the right.

By D7 the clinical situation allowed us to continue treatment in the general ward. On D8, a clear improvement on radiological findings and gas exchange was noted. The microbiological screening remained negative, and so, we proceed therapy with only quinine sulfate.

By D11 hemoglobin was 9.2 g/dL, with no leukocytosis or thrombocytopenia, and renal function, bilirubin and CRP normalized or continued to improve. Plasmodium on ticks mear remained negative. Abdominal ultrasound excluded pathologic findings.

The patient lived the hospital with a good general condition, with permanent apyrexia and without need for oxygen supply. On a subsequent ambulatory revision, a completely normal clinical status was verified.

Malaria presentation is very unspecific so alternative and more frequent diagnoses should be excluded, such as severe pneumonia, meningitis, hemorrhagic fevers, salmonellosis, viral hepatitis and dengue. Fever is common and should be treated with paracetamol, to minimize bleeding diathesis. It responds poorly to antipyretics and physical measures can be necessary.

Imported malaria, in the beginning rarely follows the classical pattern of tertian or quartan fever, which appears only after a few cycles when synchronization occurs. Additional symptoms include chills, headache, malaise, nausea, vomiting, diarrhea, abdominal pain and myalgia. Splenomegaly is an inconstant finding. In practice, malaria should be suspected in any febrile individual returning from tropics, especially if coexisting anemia, thrombocytopenia or cytolysis.

10 % of all cases have a malignant evolution. These are mostly induced by P. falciparum and may follow a explosive course with 50 % of deaths occurring in the first 24 hours. 5

Diagnosis is made by direct demonstration of parasites in blood. Parasitaemia should be determined initially, at D3, D7 and D28, to assess severity, therapy monitoring and late failures detection. 6

Agent detection can imply repeating tests at 12 h intervals, but is generally accepted treating patients empirically if suspicion remains high.

Malaria is a paradigmatic example where the early therapy and intensive monitoring brings benefits.

ARDS is defined by acute onset of bilateral pulmonary infiltrates in the absence of heart failure and a PaO 2 /FiO 2 ≤ 200 mmHg.

The absence jugular engorgement, hepatojugular reflux, peripheral edema and the typical “butterfly” infiltrates and cephalic pulmonary blood redistribution on chest x-ray, don't support cardiogenic edema. These parameters helped us to guide the fluids supplementation, without jeopardize gas exchange. However, alveolar-capillary damage really favors pulmonary edema formation.

Non-cardiogenic pulmonary edema rarely occurs with other species then P. falciparum.

Quinine sulfate is the drug of choice for severe malária, but caution should be taken in those patients with a family history of sudden death or long QT by its intrinsic arrhythmogenicity. Glocunato form is even more pro-arrhythmic.

Severe and recurrent hypoglycemia can result from hyperinsulinism induced by quinine/quinidine, malarious toxins or massive parasitism.

Renal failure, usually oliguric, rarely requires dialysis support and reverses in days.

Thrombocytopenia is common, but rarely contributes to hemorrhagic diathesis. Anemia is induced by parasitic hemolysis.

The fever increases during the first two days but should disappear after 48 hours of treatment.

The efficacy of treatment must be verified by microscopic examination of the blade. The degree of parasitaemia decreases 90 % in 48 hours and must be zero at D3.

The actual case illustrates the counsequencies of preventive measures failure, such as chemoprophylaxis.

If a parasitaemia score of 5 % reflects severity, the 43 % presented by out promised a complicated evolution, as was the case with the installation of successive failures that culminated in ARDS.

The inability to microscopically characterize the type of Plasmodium, do limited therapy institution. Results of the BinaxNOW® test, showing a single band for P. falciparum antigen, comes later. Genomic identification by polymerase chain reaction (PCR) is another available mean to identify the Plasmodium.

Compared with PCR, BinaxNOW® test showed a sensitivity of 94 % for detection of P falciparum and 84 % for other species, with overall specificity of 99 %.(7,8)

Multiorgan dysfunction, led us to admit secondary sepsis superposed on malaria, influencing the strategy.

Despite severity of the condition and the limited clinical experience, admission to a HDU capable of monitoring and early warning to complications, associated with elected conduct, proved critical to reverse the various dysfunctions, allowing the avoidance of mechanical ventilation.

Although relatively rare in Portugal, the clinical picture of malaria tends to change with progressive flow of people between countries with multiple affinities, as is the case of Portugal with African ex-colonies.

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• Open access
• Published: 10 July 2024

Examining geographical inequalities for malaria outcomes and spending on malaria in 40 malaria-endemic countries, 2010–2020

• Angela E. Apeagyei 1 ,
• Nishali K. Patel 1   na1 ,
• Ian Cogswell 1 ,
• Kevin O’Rourke 1 ,
• Golsum Tsakalos 1 &
• Joseph Dieleman 1  

Malaria Journal volume  23 , Article number:  206 ( 2024 ) Cite this article

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While substantial gains have been made in the fight against malaria over the past 20 years, malaria morbidity and mortality are marked by inequality. The equitable elimination of malaria within countries will be determined in part by greater spending on malaria interventions, and how those investments are allocated. This study aims to identify potential drivers of malaria outcome inequality and to demonstrate how spending through different mechanisms might lead to greater health equity.

Using the Gini index, subnational estimates of malaria incidence and mortality rates from 2010 to 2020 were used to quantify the degree of inequality in malaria burden within countries with incidence rates above 5000 cases per 100,000 people in 2020. Estimates of Gini indices represent within-country distributions of disease burden, with high values corresponding to inequitable distributions of malaria burden within a country. Time series analyses were used to quantify associations of malaria inequality with malaria spending, controlling for country socioeconomic and population characteristics.

Between 2010 and 2020, varying levels of inequality in malaria burden within malaria-endemic countries was found. In 2020, values of the Gini index ranged from 0.06 to 0.73 for incidence, 0.07 to 0.73 for mortality, and 0.00 to 0.36 for case fatality. Greater total malaria spending, spending on health systems strengthening for malaria, healthcare access and quality, and national malaria incidence were associated with reductions in malaria outcomes inequality within countries. In addition, government expenditure on malaria, aggregated government and donor spending on treatment, and maternal educational attainment were also associated with changes in malaria outcome inequality among countries with the greatest malaria burden.

Conclusions

The findings from this study suggest that prioritizing health systems strengthening in malaria spending and malaria spending in general especially from governments will help to reduce inequality of the malaria burden within countries. Given heterogeneity in outcomes in countries currently fighting to control malaria, and the challenges in increasing both domestic and international funding allocated to control and eliminate malaria, the efficient targeting of limited resources is critical to attain global malaria eradication goals.

Substantial gains have been made in the fight against malaria in the past 20 years. According to the Global Burden of Disease study, between 2000 and 2021 the global incidence of malaria fell by an estimated 21.1%, while malaria mortality decreased by 32.6% [ 1 ]. These gains have been made in large part because of increased coverage of malaria treatment, insecticide-treated nets (ITN), indoor residual spraying (IRS), and chemoprevention, notably in sub-Saharan Africa, where malaria transmission remains the most pronounced [ 2 ]. Despite this, recent progress towards global malaria elimination has largely stalled due to competing domestic health priorities [ 3 ], plateauing donor funding [ 4 ], disruption in control and treatment activities due to the COVID-19 pandemic [ 5 , 6 ] and inequities in burden, coverage, and utilization of services particularly in hard-to-reach populations and at the geographical margins [ 5 , 7 , 8 , 9 ].

Global health initiatives increasingly emphasize health equity as a key determinant to achieving universal health coverage. In the case of malaria, the World Health Assembly endorsed the Global Technical Strategy for Malaria, which advocates for the inclusion of malaria interventions as part of universal health care and acknowledges the importance of adapting the malaria response to suit the context in each country [ 10 ]. Geographic gradients and progress towards equity in malaria control have been documented in several broad strands of the literature. For example, multiple studies using population-based surveys have demonstrated disparities in malaria transmission, coverage and outcomes, where outcomes capture the result of interventions, such as incidence and case fatality rates, across socioeconomic status [ 11 , 12 , 13 ]. While the drivers of inequality in malaria outcomes are routinely examined as part of national control programs, less frequently evaluated are the drivers of geographical differences in treatment outcomes among endemic countries, with available evidence mostly comprising of national or regional assessments of spatial variation [ 14 , 15 , 16 , 17 ].

While domestic and international financing for malaria rose considerably between 2000 and 2016 [ 18 , 19 ], investments in malaria still fall short of targets set by the World Health Organization. The overall funding gap has increased from $2.6 billion in 2019 to $3.5 billion in 2020 and $3.8 billion in 2021 [ 20 ]. Achieving progress in the equity of malaria outcomes between and within countries requires efficient use of investments and the optimal allocation of resources in malaria control and elimination programmes [ 19 , 21 , 22 ]. To date, however, the association between malaria spending and the inequitable distribution of malaria outcomes within countries has not been comprehensively assessed.

In this study, state-level estimates among 40 malaria-endemic countries are used to demonstrate the magnitude and drivers of inequalities in malaria. Additionally, the relationship between inequality and malaria spending from domestic and foreign sources, disaggregated malaria spending by functional area, maternal education, health systems performance, economic status, and infectious disease risk measured at the country level are assessed. The study findings highlight associations between malaria outcome inequality and spending on malaria and demonstrate how spending through different mechanisms might lead to greater health equity.

This analysis was conducted in 40 malaria-endemic countries with the greatest incidence rates defined in this study as countries with incidence rates greater than 5000 cases per 100,000 in 2020 (see Table  1 ). The analysis focuses on this subset of endemic countries, as geographic disparities could indicate limited access to necessary prevention and treatment to malaria at the state level. The study focuses on high endemic countries and exclude low endemic countries because countries with little malaria incidence tend to have high GINI values not because of great inequality per se but largely because their malaria incidence is low in general within the country.

Definition of geographic disparities

Data on total malaria cases (combined Plasmodium falciparum and Plasmodium vivax ) and deaths ( P. falciparum ) at the first administrative level (admin1) from 2010 to 2020 were obtained from the Malaria Atlas Project (MAP) ( www.map.ox.ac.uk ). Using these data, malaria incidence, mortality, and case fatality for each first administrative unit were calculated. To estimate incidence and mortality rates, the number of cases or deaths (numerator) was divided by the population (denominator). To estimate ( P. falciparum ) case fatality ratios, mortality rates were divided by incidence rates to provide a population-based indicator of survival. These values were then used to compute the outcome measures of interest for this study.

For our outcome measures—incidence and case fatality—the Gini coefficient (also known as the Gini index) derived from the Lorenz curve [ 23 ] was adapted as a proxy for the relative difference in malaria incidence or case fatality within each malaria-control country (Appendix Section B). Although the Gini coefficient is most commonly used in studies on wealth and income inequality, it has been employed to analyse health disparities, including disease burden [ 15 , 17 , 24 ], life expectancy [ 25 ], inequality in particulate matter 2.5-related health outcomes [ 26 ], and DTP3 vaccine coverage [ 27 ]. The Gini coefficient is defined as:

where \(G\) is the Gini coefficient, \(i\) is the admin1 unit of interest, \(N\) is the number of admin1 units in a given country, \(P_{i}\) is the cumulative proportion of the population in the \(i{\text{th}}\) unit, and \(C_{i}\) is the cumulative proportion of malaria outcomes in unit \(i{\text{th}}\) unit. For each of the outcomes (incidence and case fatality), the Gini coefficient was calculated for each country and year by first ranking subnational units in decreasing order of the variable. The values of the Gini coefficients range from 0 in complete equality to 1 in complete inequality. When applied to malaria incidence, a Gini coefficient of 0 represents perfectly equitable distribution of malaria incident cases within countries and a Gini coefficient of 1 is interpreted as all malaria incident cases concentrated in one subnational unit. When applied to malaria case fatality, a Gini coefficient of 0 indicates that deaths due to malaria are equal across subnational units, whereas a coefficient of 1 indicates that deaths due to malaria are concentrated in one subnational unit.

Malaria spending

The main predictor variables are total, government, and disaggregated malaria spending (i.e., spending broken down by program type). Data on total, government, and disaggregated malaria spending from 2010 to 2020 were extracted from the Institute for Health Metrics and Evaluation (IHME)’s Financing Global Health databases [ 28 , 29 , 30 , 31 ].

Total malaria spending consisted of government health expenditure (GHE), out-of-pocket (OOP) expenditure, prepaid private (PPP) expenditure, and development assistance for health (DAH) for malaria. Total malaria spending data were real currency converted to 2021 USD and expressed as spending per person in the population-at-risk. Spending per person at risk population was defined as total malaria spending divided by the World Malaria Report estimates of population at risk. The World Malaria Report estimates of population at risk is calculated using proportion of population at high, low, and no risk of malaria transmission provided by country-level national malaria control programmes.

Government malaria expenditure as a proportion of total malaria spending was included as a covariate, to provide an indication of a country’s social and political decisions as to how much funding should be allocated to malaria relative to the overall health budget.

Government expenditure on malaria and DAH for malaria were disaggregated by programme type [ 18 , 31 ], including insecticide-treated nets (ITNs), indoor residual spraying (IRS), anti-malarial medicines, drug resistance, other vector control, human resources and technical assistance (HRTA), procurement and supply management (PSM), planning, administration, and overheads (PAO), infrastructure and equipment (IE), monitoring and evaluation (ME), other health systems strengthening, and other malaria programmes.

For the purpose of this analysis, disaggregated spending categories were combined to create three variables that captured spending on prevention, treatment, and health systems strengthening (Table  2 ). Programmes from which spending was categorized as prevention included ITNs, IRS, and other types of vector control. Programmes from which spending was categorized as treatment included anti-malarial medicines and drug resistance. Programmes from which spending was categorized as health systems strengthening (HSS) included HRTA, PSM, PAO, IE, ME, and other health systems strengthening. The three disaggregated spending variables were expressed as proportions of aggregated government expenditure on malaria and DAH for malaria.

Other drivers of geographic disparities

The study analyses controlled for other potential socioeconomic and demographic drivers of geographic disparities ( \(X_{it}\) ) in malaria outcomes (Table  2 ). Covariates include the gross domestic product (GDP) per person, age dependency ratio, the Healthcare Access and Quality (HAQ) Index, average maternal education, population-weighted mean temperature, and national malaria incidence (Table  2 ). The covariates included were primarily informed by a conceptual framework from the WHO’s commission on the Social Determinants of Health (SDoH). This framework captures the primary structural and socioeconomic inputs that drive equity in health and wellbeing. Additional covariates were also included from the literature based on their established importance with health outcomes and the outputs of interest [ 32 , 33 , 34 , 35 , 36 , 37 , 38 ].

Statistical analyses

Overall, malaria spending and GDP per person were log-transformed. These two variables were log-transformed to normalize the distribution and to allow for plausible interpretation of their respective coefficients [ 39 ]. From 2010 to 2020, within-country disparities in malaria over time are found and and the trends in disparities over time plotted. Furthermore, a panel dataset for 40 malaria-endemic countries from 2010 to 2020 is constructed. The following equation was used to estimate overall geographic inequality in malaria outcomes in order to quantify associations with changes in within-country geographic disparities.

where the Gini index, \(g_{it}\) , in country \(i\) at year \(t\) is a function of total spending on malaria ( \(TotalMalSpend\) ). Using this equation, when the independent variable is log transformed \(\beta_{1}\) —the coefficient of one of our variables of interest—can be interpreted as a 10% increase in total malaria spending is associated with a \(\beta_{1} \times {\text{log}}\left( {1.10} \right)\) unit change in the dependent ( \(g_{it}\) ) variable. For government and disaggregated malaria spending, the other variables of interest, the coefficient can be interpreted as a 10% increase in the independent variable is associated with a \(\beta \times 10^{2}\) percent change in the dependent variable. The standard errors of the coefficients were adjusted for using Huber-White robust adjustment to control for heteroscedasticity across panels and are clustered by years to address any serial correlation over time. Fixed effects on country ( \(\alpha_{i}\) ) and year ( \(\gamma_{t}\) ) were used to account for any unobserved confounding factors which vary by country and over time. It is important to note that these evaluations are all descriptive and not causal. All analyses were completed using R (version 4.2.1).

The study found variation in geographic disparities in malaria incidence and case fatality across malaria-endemic countries (Fig.  1 ). In 2020, values for within-country Gini coefficient ranged from 0.06 to 0.73 for incidence and 0.00 to 0.36 for case fatality. Liberia, Burkina Faso, and Benin had the least incidence inequality (< 0.076), while Djibouti, Yemen, and Guyana had Gini coefficients greater than 0.42 (Fig.  1 B). Inequality appears to be less pronounced when case fatality is considered. For case fatality, Djibouti, The Gambia, and Papua New Guinea had the least inequality (< 0.0085) whereas Mauritania, Guyana, and Mali had coefficient values greater than 0.32 (Fig.  1 C). Countries with the lowest total malaria spending per person at risk—including Somalia, Yemen, Madagascar, and South Sudan—had consistently high incidence inequality levels (Fig.  1 A).

Comparison between total malaria spending ( A ) and inequality in incidence ( B ) and case fatality ( C ), 2020

Country inequality time trends between 2010 and 2020 are illustrated in Fig.  2 . Overall, country inequality decreased during the study period on average. The Gini coefficient peaks at 0.81 for incidence and 0.75 for case fatality throughout the time series. Across the two outcomes, countries have varying baseline values with greater variation in values for the Gini coefficient for case fatality than for incidence. Some countries also experience steep gradients at specific time points such as Djibouti, Guyana, Madagascar, and Somalia while other countries maintained relatively constant coefficients through the entire time spectrum including Cameroon, Central African Republic, Liberia, and Papua New Guinea.

Country-specific trends in inequality, 2010–2020. There were no deaths reported in all Djibouti subnational units in 2011 and 2012

Table 3 summarizes the analysis exploring potential determinants of inequality using models to assess changes within a country, over time, controlling for all time-invariant country characteristics. The study found significant associations for total malaria spending, proportion sourced by government, proportion spent on health systems strengthening, national malaria incidence, Healthcare Access and Quality Index, maternal education, and population-weighted mean temperature.

A 10% increase in total malaria spending per person at risk was associated with 0.002 (95% confidence interval: 0.002–0.007) and 0.003 (0.002–0.011) unit decrease in incidence inequality and case fatality inequality, respectively. Spending on health systems strengthening was associated with a decrease of 11.5% (2.7–20.3) in case fatality inequality. Additionally, national malaria incidence rate was associated with decreases in both incidence and case fatality inequality. In perspective, every increase of 1,000 per 100,000 in incidence is associated with 0.274% (0.152–0.397) and 0.289% (0.087–0.491) decreases in incidence and case fatality inequality, respectively. A one-unit change in the healthcare access and quality index was associated with a 1.1% (0.2–2.0) decrease in incidence inequality. Conversely, government malaria expenditure was associated with an increase of 19.8% (10.4–29.1) in case fatality inequality. A one-degree increase in population-weighted mean temperature was related to a 2.8% (0.2–5.5) increase in incidence inequality. Finally, an additional year of maternal education was associated with a 6.4% (2.0–10.8) increase in incidence inequality.

We further stratified countries by burden of malaria to test for a possible differential effect of malaria spending on outcome inequality. The national incidence rate in 2020 ranged from 0.05 in Senegal to 0.38 in Benin. Countries in the top 50th percentile for burden of malaria included the Solomon Islands and 19 countries in sub-Saharan Africa with an incidence rate greater than 0.228 in 2020. Among high-burden countries, this sensitivity analysis indicated that higher total malaria spending and average maternal education were associated with reductions in malaria outcome inequality. Additionally, government contribution to malaria spending and national malaria incidence were associated with decreases in incidence inequality. Inversely, proportionally higher spending on treatment, GDP per capita, and the age dependency ratio were associated with increases in case fatality inequality. Further, broader development (i.e. GDP per capita and working age population) and environmental conditions (i.e. population-weighted mean temperature) are associated with increases in case fatality and incidence inequality, respectively.

Two additional sensitivity analyses were performed. The first replicated the main analysis using country fixed effects, as opposed to country and time fixed effects, as an alternative model parameterization to assess the potential impact of time. The second used the Gini coefficient for mortality as an alternative outcome measure to case fatality inequality. Although case fatality may be a stronger and more focused indication of the efficacy of and inequalities in spending on treatment, mortality rates may be a stronger indicator of the burden of malaria within the entire population. Both analyses produced similar results to the primary analyses. However, a greater proportion of total spending that is sourced from governments was associated with a decrease in mortality inequality. The results of these sensitivity analyses are presented in Appendix Section C.

The study investigated country-level drivers and characteristics associated with a measure of inequality for two malaria outcomes across 40 malaria-endemic countries. Total and government malaria spending, spending on health systems strengthening for malaria, maternal education, and population-weighted mean temperature were identified as important drivers of inequality in malaria outcomes within countries. The findings from the study showed how malaria elimination efforts can benefit from quantifying the variation in these drivers of inequality across population groups and geographic areas. A more precise understanding of the patterns of malaria burden can inform government decision-making, while also helping external funders allocate resources to those areas with the greatest need.

This study is the first to demonstrate how malaria spending through different mechanisms can impact the inequality of disease incidence and case fatality within countries; previous studies focused solely on quantifying geographic variation within individual countries, or variation in malaria-related inequality at the regional level [ 15 ]. This study is also the first to apply the Gini index to all countries where malaria continues to cause significant health burden over time. The practical advantage of using the Gini index is that it is a widely used, simple, and standardized measure that is not sensitive to extreme values in malaria outcomes. As such, use of the Gini index in this context provides a comprehensive assessment from which individual countries can assess their performance in malaria elimination against other countries with similar endemicity.

The results from the study highlight some inequality in malaria burden, with average values of the Gini coefficient being 0.20 and 0.18 for incidence inequality and case fatality inequality, respectively, in 2020. While inequality has declined between 2010 and 2020, there is still remains a need to prioritize reducing the malaria burden equitably within countries. The results are in line with previous studies of inequality in malaria outcomes, but the values for within-country malaria inequality in this study are generally lower than those shown in other studies (Fig.  2 ). For example, a cross-sectional analysis of malaria incidence inequality within Sierra Leone, Nigeria, Ghana, and Burkina Faso found Gini coefficient values ranging from 0.17 to 0.30 between 2015 and 2017 [ 15 ], whereas our study had a range of 0.11 to 0.21 for the same countries. Studies using more granular epidemiological surveillance data at the district level also found comparable values for the Gini coefficient for malaria incidence [ 14 , 16 ].

Malaria morbidity and mortality are strongly influenced by the performance of health systems. The findings suggest an association between a higher proportion of malaria spending on health systems strengthening and improved equity in case fatality. Additionally, the study found that a higher proportion of spending on malaria treatment increased inequities in case fatality in high-burden countries; this may be an indication of differential access to malaria treatment between states. The success of malaria control and elimination programmes is acknowledged to be handicapped by the ability of health systems to deliver high-quality interventions that reach the full population-at-risk [ 40 , 41 , 42 ]. Further, work by Sahu et al . found health systems strength to be predictive of reductions in malaria burden [ 43 ], particularly in high-burden countries. These countries may see the greatest benefit from systems strengthening [ 44 ] and the integration of a people-centred approach [ 42 ].

Additionally, access to high-quality healthcare has been recognized as both key to improving healthcare delivery and as a necessary driver of universal health coverage. The study found an association between access to quality healthcare (measured using the HAQ Index) and incidence inequality in the main analysis. This finding is aligned with work by O’Meara et al . that reinforced the importance of primary care—and the proximity to primary care—to malaria outcomes [ 45 ], as well as other work showing lower malaria mortality rates in more prepared health centres in Burkina Faso [ 46 ], Uganda [ 47 ], Kenya, Namibia, and Senegal [ 48 ].

There are some important limitations of this work. To start, the estimates of domestic malaria spending used in this analysis [ 31 ] were generated using country-reported data, which is subject to data gaps such as missing data and incomplete documentation and, therefore, required modelled estimation. Interpreting malaria spending estimates is also complicated. For example, while high spending can be attributed to a heavy malaria burden, it may also be influenced by wealthier nations with less burden and their efforts towards eliminating malaria entirely. As such, national spending on malaria treatment, prevention, and health systems strengthening as a proportion of total malaria spending were transformed.

Additionally, the study does not quantify inequality among countries with low national incidence or incidence concentrated in specific areas of countries. This is because Gini coefficients could be skewed by small number bias (i.e. few admin1 units with malaria burden), systematically biasing estimates towards inflated Gini coefficients [ 49 ]. As such, the analysis was restricted to relatively high-burden countries only (Tables  1 and  4 ). While the Gini coefficient is a useful quantitative descriptor of malaria inequality, it is important to note that these values do not represent absolute differences in malaria outcomes and that different distributions of malaria outcomes within countries can produce the same Gini coefficient. Future applications of the Gini coefficient as a standardized measure of disease inequality could consider its use alongside detailed qualitative data exploring determinants of underlying geographic heterogeneity.

The series analysis was restricted to 2010 to 2020 as admin1 level data of incident cases and deaths from MAP were only available for this period. This study also employs cross-sectional methodologies for time series analysis, which does not imply causality between the predictors and outcomes. Therefore, it is important to note that these evaluations are all descriptive and not causal. One of the outcomes in the study was defined as ‘spending per person at risk population’ the authors acknowledge that the level of risk people face may vary because of inequities but the scope for this study does not allow for further investigation of that variation. Nevertheless, the findings provide an important foundation for initiating discussions on plausible causal theories in settings characterized by high inequalities in malaria burden.

Inequalities have been widely acknowledged as barriers to achieving global and national targets in malaria programs. To realize global malaria elimination, routine surveillance activities should include inequality monitoring at lower geographic levels from which methods to address existing gaps can be drawn. This paper provides an important policy message with implications for both national governments and the international community. Results from this study highlight the responsiveness of geographic inequalities in malaria incidence and case fatality to the way in which financial resources for malaria are allocated, as well as to broader drivers of economic development. While the finding that more funding improves malaria outcomes is not new, the finding that increased funding may also reduce geographic inequalities is new. This highlights the potential double impact of malaria programme investments. It is, therefore, essential that countries controlling for malaria continue to prioritize efficiency in their resource investments to be able to improve upon their malaria outcomes and geographic inequalities despite limited availability of additional financial resources. Furthermore, even though some of the results suggest that a greater proportion of spending on malaria treatment is associated with greater case fatality inequality, this is not suggesting that treatment should not be prioritized but rather that ensuring equity in treatment availability should be further prioritized.

The results presented in this paper highlight the large heterogeneity in malaria outcomes between 2010 and 2020 within malaria-endemic countries. The analysis further shows the high impact of allocating greater resources towards health systems strengthening and improving healthcare access and quality in the reduction of inequality of malaria burden within countries. This indicates the potential double impact of stronger health systems and in addressing distributional challenges related to the attainment of elimination and eradication goals across countries.

Availability of data and materials

The data used in the analysis is available in the supplemental appendix.

Abbreviations

Gross domestic product

Healthcare Access and Quality index

Health systems strengthening

Malaria Atlas Project

Insecticide-treated nets

Indoor residual spraying

Human resources and technical assistance

Procurement and supply chain management

Planning, administration, and overheads

Infrastructure and equipment

Monitoring and evaluation

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This work was funded by the Bill and Melinda Gates Foundation (Grant No. INV-005967).

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Angela E. Apeagyei and Nishali K. Patel are co-first author.

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Institute for Health Metrics and Evaluation, 3980 15th Ave NE, Seattle, WA, 98195, USA

Angela E. Apeagyei, Nishali K. Patel, Ian Cogswell, Kevin O’Rourke, Golsum Tsakalos & Joseph Dieleman

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NP: conceptualization, methodology, formal analysis, writing—original draft, writing—review and editing. AEA: conceptualization, methodology, writing—original draft, writing—review and editing, supervision, validation. IC: data curation, writing—reviewing and editing. KO: writing—original draft, writing—reviewing and editing. GT: supervision, project management. JLD: conceptualization, methodology, supervision, validation, writing—original draft, writing—reviewing and editing.

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Correspondence to Angela E. Apeagyei .

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Apeagyei, A.E., Patel, N.K., Cogswell, I. et al. Examining geographical inequalities for malaria outcomes and spending on malaria in 40 malaria-endemic countries, 2010–2020. Malar J 23 , 206 (2024). https://doi.org/10.1186/s12936-024-05028-4

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Received : 08 September 2023

Accepted : 26 June 2024

Published : 10 July 2024

DOI : https://doi.org/10.1186/s12936-024-05028-4

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