Case of the Month

June 2013

Dr Jeannine van Lochem, SASTM

In the early evening of a day in mid-April, (“Day 1”), a 60 old male, British national, presents to a small clinic on a mine, approximately 70 kilometres west of the Malian border, in Senegal, West Africa.

Patient complains that he “...feels like he is burning up,...” and has lower abdominal and back pain over kidney region. He is nauseas, not vomiting, but has no appetite.

Vital signs:

BP: 123/86 mmHg; Pulse: 98 beats/minute; Respiratory rate: 22 beats/minute;

Temp: 39.3 C; SpO2: 98%

On examination: Lower abdominal and renal angle pain and tenderness, nil else remarkable.

Question 1: What else do you want to know?

Answer to Q1

  • Pre-existing disease / illness
  • Past surgical history
  • Chronic medication
  • Malaria prophylaxis
  • Current vaccine cover
  • Travel history - where has he been in the last 12 months
Case Continued

The patient had a laparotomy for unknown reason 15 years ago and a cholecystectomy 5 years ago.

No chronic medication and no malaria prophylaxis.

Vaccine cover - all childhood vaccines covered plus Yellow Fever, Meningococcal disease, Typhoid, Hepatitis A and B.

Lives in Scotland. Been working on this mine for the last two years on a 6 weeks on 2 weeks off roster.

Side room laboratory examination reveals:

Dark, concentrated urine

Urine Dipstick:


Blood Glucose: Not done.

Malaria Rapid Test for P falciparum [HRP2]: Negative

No other laboratory investigations possible on site (blood can be sent on a twice weekly, two-hour charter flight to a private laboratory in Dakar).

Question 2: What is your differential diagnosis based on the available clinical and laboratory information?

Answer to Q2

  • Malaria
  • Pyelonephritis
  • Prostatitis
  • Basal pneumonia
Case Continued

The patient reveals that he has been seeing a urologist for “bladder problems” on and off for some time - this had not been mentioned before.

A diagnosis is made: “A Urogenital Infection”

Medication prescribed:

  • Ciprofloxacin 500mg twice a day (14)
  • Paracetamol 500mg three times a day (10)
  • Vitamins + Minerals x 10
  • Metoclopramide: 10mg x 6 as needed for nausea
  • Patient to drink lots of water - which he does not like doing…

Day 2:

At midday the patient is seen in the communal dining room - he says he is feeling a lot better - and he is apyrexial.

Day 3

The patient returns to the clinic mid-afternoon for a follow up visit: He is “… feeling terrible again….”

Vital signs: B/P 112/90; Pulse 91 beats per minute; Temperature 39.2 C ; Oxygen saturation 96%.

Question 3: Which test MUST you repeat now?

Answer to Q3

Malaria rapid antigen test

Case Continued

A repeat Malaria test: Negative

Urine test
PH 6
Blood +++
Rest of parameters negative or within normal limits.

Patient management:


  • Normal Saline infusion: 200ml.
  • Paracetamol 1g IVI.
  • Instructed patient to drink more fluids. Patient under observation in clinic for the day. Patient did not urinate the whole day, still said he is not a water drinker, he did bring a soft drink with, which he did not drink because he was sleeping the whole day.

@ 16h52 - Temperature: 38.8C. Patient booked off, but sent back to room to overnight.

Day 4

Patient back in clinic for follow up.

Vitale signs: B/P 100/57; P 63 beats per minute; T 36.3C; Oxygen saturation 98%.
Urine test: SG 1025; PH 6; Rest of results negative / non-remarkable.

Recommenced infusion, push oral fluids. At midday the temperature is normal at 36.4C; Mid-afternoon the vital signs are essentially normal with a normal blood pressure of 122/78 but the patient complains about a lot of pain over his kidney area again - more, more painful on the left side. The patient has been apyrexial all day and it is decided to continue his antibiotics and maintaining a good urine flow.

Question 4: In an ideal setting - what would you have requested at this point in time?

Answer to Q4

  1. Nothing – the patient is apyrexial, urine has cleared up according to dipstick test - looks as if antibiotics is beginning to work. However,
  2. Recurrence of left renal angle pain is of some concern, so would have liked to do: Urine for microscopy and culture, ultra-sound abdomen / kidneys and bladder, full blood count, malaria screen and CRP, urea and electrolytes, blood cultures.

The patients’ temperature has settled and vital signs normalized but the on-going loin pain is reason for concern in a patient with a urological history.

Case Continued

Day 5

The patient presents himself to the clinic for review stating that he feels 100% better, except for a headache.

Vital signs: B/P 123/73; Pulse: 70 beats per minute; T 36.6 C; Oxygen saturation 98%.

Urine test: Macroscopically clear. SG 1010; PH 6; Blood +; Glucose Trace. Bilirubin +; Leucocytes+.

Medication: Paracetamol for the headache.

In the mid-afternoon a mild temperature of 37.9C is noted.

There is a roster charter flight to Dakar the next day.

Question 5: Would you -

  1. Continue treatment as is?
  2. Change the antibiotics to cover the on-going renal pain?
  3. Send blood and urine to Dakar for analysis in a full-scale private laboratory?
  4. Refer the patient to Dakar to see an Urologist?
  5. Send the patient back to the United Kingdom to see his own urologist?

Answer to Q5

It was decided to refer the patient to Dakar to see an Urologist in the light of the recurrence of mild fever and the recurrence of / on-going blood in his urine. Sending the biological specimens only does not make sense - if the results require sophisticated treatment the patient would have to wait for the next charter four days later or require a dedicated air ambulance at considerable expense to all.

The patient refuses to see a Urologist in Dakar - insists on going home to his ‘own doctor’.

The patient is considered well enough to fly home on his own on a commercial flight.

The patient arrives back in the UK without further ado but feels unwell enough to consult his doctor.

Question 6: If you were the ‘own doctor’ in the UK, what would you consider as the top five likely diagnoses in this patient?

Answer to Q6

  • Malaria
  • An infection of the urogenital system
  • A gastrointestinal infection e.g. colitis, typhoid.

Question 7: Assuming a non-remarkable examination and knowing the patients history as described earlier, which laboratory investigations would you request?

Answer to Q7

  • Urine dipstick followed by microscopy and culture
  • Full blood count
  • malaria screen (microscopy and rapid antigen test)
  • CRP
  • Urea and electrolytes
  • Blood cultures
  • ultra-sound abdomen/kidneys and bladder.

The laboratory results reveal:

  • Full blood count: Normal except for a low platelet count of 88 x 109/L
  • Raised Bilirubin: 24
  • Malaria smear: Positive for Plasmodium ovale
  • Rapid antigen test for P falciparum and P ovale: Both negative

Question 8: How will you treat the patient?

Answer to Q8

Treat the acute infection with oral artemether / lumefantrine.

Check for Glucose-6-phosphate dehydrogenase (G6PD) deficiency

Treat with Primaquine 15mg / day for 14 days to eradicate liver hypnozoites

Back on site you receive a report that the patient received Riamet® (Co-artem) and then Primaquine from the treating doctor in the UK and pending a repeat full blood count, malaria smear and ultra-sound abdomen, will be returning to site in a week.

Question 9: Are you satisfied that the patient received the correct treatment and that he is fit to return to site?

Answer to Q9

Riamet® is the trade name for Coartem® produced by Novartis in Europe. Both contain artemether / lumefantrine. It is therefore considered adequate treatment for the acute phase of both uncomplicated P falciparum and P ovale malaria. Primaquine must be used to eradicate any hypnozoites in the liver to avert a relapse weeks to months later.

Primaquine cannot be used in persons who are fully G6PD deficient and all persons in whom the administration of Primaquine is considered must be tested for enzyme deficiency first. However, African patients tend to have less severe mutations than those of Asian origin, and alternate regimens of Primaquine should be discussed with a Travel Health or Infectious Diseases specialist for advice.

It is best practice to do a repeat blood screen and malaria smear to ensure that all parasites have gone and make sure the platelet count has returned to normal and that the haemoglobin has remained within normal limits. There is no specific benefit in performing an ultrasound of the liver.

It is best to make double sure that all clinical and laboratory parameters have normalized before allowing a previously ill patient back on to a remote site with limited medical facilities.

Question 10: Why is confirmation of the actual diagnosis in this case of particular importance to you as the medical provider on this remote mine site in Senegal?

Answer to Q10

It is common knowledge that 95% of the malaria in Sub-Saharan Africa is caused by Plasmodium falciparum, the most lethal form of malaria and responsible for the majority of deaths due to malaria in the world.

Non-falciparum malaria is known to occur in the region but not routinely looked for by either clinicians or laboratory technicians as it very scarce and seldom the cause of complications and death in otherwise well patients.

Rapid antigen tests that are single species specific will not detect non-falciparum malaria if intended solely for the detection of P falciparum. Rapid antigen tests that can detect multiple species are generally much less reliable and their interpretation prone to mistakes.

It is therefore of epidemiological and public health importance to confirm the diagnosis as this may be the index case highlighting the fact that there is non-falciparum malaria on site and that it might be prudent to change the malaria management protocol on site, assuming that this particular patient did not contract P ovale elsewhere in the world where P ovale is well known to occur.


Plasmodium ovale malaria is not commonly diagnosed in South Africa

As Plasmodium falciparum malaria is the most common, as well as the potentially most lethal form of malaria in Sub-Saharan Africa, we tend to focus on the clinical diagnosis, laboratory investigation and management of acute uncomplicated and complicated falciparum malaria in travel health teaching and discussions in South Africa.

This case puts the focus on the other, somewhat ‘neglected’ malaria species on the continent.

In our travel health practice we consult approximately 3 500 travellers a year and, on remote sites in Sub-Saharan Africa, take care of roughly 600 expatriates and 5 700 national client employees on any given day of the year.

We annually diagnose about 280 malaria cases on the remote sites (implying that less than 1% of the total number of persons under our care in malaria endemic areas are diagnosed with malaria) and perhaps 10 in returned travellers and medevac cases in our Johannesburg based clinic.

We have been doing this for more than fifteen years.

This is the first case of non-falciparum malaria emanating from one of our sites in which it can be considered that we ‘missed’ the diagnosis. In total we are aware of about three cases of non-falciparum a year amongst our entire client base, including that of an international health insurance company for whom we provide medical cover. Most of these cases originated from Mozambique and the actual diagnosis of non-falciparum malaria could not be confirmed in more than one of them, illustrating the fact that the diagnosis of non-falciparum malaria is often not an easy one in a non-endemic area.

We are aware of one other case - the patient worked on a remote site in Liberia and was diagnosed with P ovale in Australia. We could however not say with certainty that he contracted the malaria on site in West Africa as he had travelled and worked in South East Asia, where P ovale is much more common, extensively.

Plasmodium ovale

Historical references istretching from the Philippines to the Gold Coast in West Africa, of what was likely Plasmodium ovale can be found in the literature from 1900 onwards. It had been reported from Indonesia and has been introduced to Vietnam, Thailand and India. Two sub-species have recently been documented: P. ovale curtisi and P. ovale wallikeri.ii

P ovaleiii is seldom seen except in Sub-Saharan Africa and some western Pacific islands (New Guinea and the Philippines). In SSA it makes up part of the less than five percent of non-falciparum malaria diagnosed annually, amongst a sprinkling of P malariae and some P vivax. P ovale has been documented in Senegal and The Gambia before. Prevalence rates in children in the Republic of Congo, Liberia, Cameroon and Gabon are in the region of 1,9% to 9% but this must be seen on the background of a prevalence of malaria of 24,5 to 30% amongst the same children. In a study in Dielmoiv , Senegal only three cases of P ovale was detected out of a total number of 162 malaria patients. All the others had P falciparum malaria and this in turn was responsible for 61% of febrile episodes recorded in the study. Other countries from which P ovale infestations had been documented include: Southern Sudan, Uganda, Zimbabwe, Ethiopia, Zambia, Tanzania and Kenya.

Sporozoites injected by the mosquito rapidly invade the liver where it matures in about 9 days. This corresponds with a prepatent / ‘incubation’ period of 12 to 20 days with a median in one study of 14 days. Hundreds of merozoites are released to invade young red cells. Some of the parasites remain behind in the liver in limbo to form hypnozoites. They may only develop into merozoites months to years later.

The merozoites in the red cells will erupt and invade a next batch of red cells after about 49 hours. After another 49 hours some of the merozoites become gametocytes.

Mosquitoes then take up these microgametocytes during a blood meal, so completing the developmental cycle in the mosquito. Sprozoites appear in the salivary glands weeks after the mosquito had become infested.

Fever spikes occur roughly every 49 hours.

P ovale malaria smears usually record low parasite counts in comparison to P falciparum and P vivax infections due to the parasites restriction to reticulocytes. This makes diagnosis by conventional smear as well as per rapid antigen test relatively difficult. Persons who have previously had P ovale may have reduced parasite levels and lower fever peaks.

Relapsing infection occurs in P ovale due to the presence of hypnozoites in the liver. These may be asymptomatic - posing a potential public health threat with the ‘silent’ introduction of the parasite in to a P ovale naïve community, such as a mine or construction camp.

A first relapse may occur 17 days after completion of treatment of the primary attack but has been recorded up to 255 days later.

Delayed primary attacks may occur up to four years after infestation of the liver due to the effect of malaria prophylaxis or treatment taking at the time of what would have been the usual primary attack.

The parasite makes use of a wide range of Anophelene mosquitoes as vectors, with A gambiae and funestus being the most likely.

The diagnosis of P ovale is normally done by microscopic examination of a Giemsa stained peripheral blood smear. It is difficult to differentiate P ovale from P vivax!

P ovale produces fewer merozoites in the red cell and does not distort / enlarge the erythrocyte as much as P vivax. It does however produce a higher percentage of ‘oval’ / elliptical red cells and more Schüffner’s stippling - for those of you that cant wait to rush out to a microscope!

Human malaria parasite species can be differentiated by making use of PCR - this should be reserved for difficult cases and use in research and is NOT intended as first in line for day to day diagnosis of malaria in the clinical setting.

Lessons Learned

The case under discussion provides an opportunity to revisit a number of well-known dictums in the diagnosis and treatment of malaria in Africa and adds a few new one’s to consider:

  • Any patient who presents with a febrile / ‘flu-like illness in a malaria endemic area has MALARIA UNTIL PROVEN OTHERWISE.
  • One negative blood smear / rapid antigen test does not exclude malaria: Repeat the test until malaria is diagnosed or another diagnosis explaining the fever and other signs and symptoms is conclusively made and laboratory confirmed.
  • A good history and comprehensive physical examination remains the basis of good medical practice – however, in this case the history of ‘urological problems’ coupled with blood and leukocytes in the urine side-room test, served as a distractor. Haemolysis caused by malaria will produce a positive dipstick for blood / haemoglobin as well as bili- and urobilinogen. Malaria should not as a rule cause a positive dipstick for leukocytes or nitrates – which is why the clinicians taking care of the case ‘saw’ the urogenital infection in their findings.
    • If the clinicians had access to the patient’s pre-deployment medical records they would have been able to compare the results of a pre-deployment medical examination with the present - this might have shown that the patient had leukocytes prior to deployment as part of an on-going chronic low-grade urogenital condition. This might have turned their attention back to another likely cause for the blood / haemoglobin and urobilinogen, e.g. malaria.
  • A travel history, current vaccine cover and whether the patient has been compliant with malaria prophylaxis is always of paramount importance in any febrile traveller as this assists in compiling a list of more and less likely differential diagnosis.
  • A comprehensive physical examination in which the clinician actively looks for signs that may explain the origin of a documented fever is essential. Important points to note include skin rashes, insect bites and eschars, lymphadenopathy, organomegaly and jaundice.
  • Bedside / side room laboratory tests play an important role in any clinical setting, more so in areas with limited medical infrastructure, such as a remote mine or construction site. In addition to malaria rapid antigen tests, basic urine dipstick screening and blood glucose levels are invaluable in every setting.
  • Malaria rapid antigen tests have revolutionized the diagnosis of malaria in individuals and the epidemiology of the disease across the African continent.
    • A good quality rapid antigen test is more accurate and reliable than poor microscopy in both the malaria endemic developing world and in laboratories in the industrialised, non malaria endemic world, benefitting febrile inhabitants of malaria endemic countries as well as ill returned travellers in non-endemic industrialised countries.
    • Rapid antigen tests have increased the standards of malaria diagnosis in the developing world, thereby contributing to the massive decrease in malaria reporting to the WHO in the last decade.
  • Despite the advantages listed in the previous bullet point, the test is subject to certain limitations that need be borne in mind at all times:
    • The rapid antigen test used must be well manufactured, correctly stored and used.
    • There are two types of rapid tests commonly used in Africa:
      • A test that detects the Histidine 2 Rich Protein of the parasite wall and,
      • A test that detects LDH produced by living parasites.
    • The single species H2RP test for P falciparum is highly sensitive and specific and the test of choice in Sub-Saharan Africa where P falciparum is rife and poses a high risk of death in non-immune travellers and immunocompromised individuals.
    • The multi-species tests that detect P falciparum, non-falciparum and mixed infections are less sensitive and specific and are more difficult to interpret correctly.
    • Because of the serious consequences that a missed P falciparum infestation may have, clinicians may choose to preferentially use the single species rapid antigen test for P falciparum only, but then run the calculated risk of missing a non-falciparum malaria, as happened in this case.
      • It is noteworthy that the laboratory in the United Kingdom detected P ovale on the malaria smear, confirmed by relatively sophisticated PCR, but that two immunochromatic tests (Rapid antigen tests) for P ovale were in any event negative…
      • Conversely, the rapid antigen tests done on the mine were intended for the diagnosis of P falciparum only; the test was repeated twice but, with hindsight not surprisingly, negative in both instances.
      • PCR is not intended as a primary method of detecting malaria in the clinical setting.
  • Look - and think! – twice whenever a patient who presents with a fever on the first day, looks and feels better on the second day: This is no reason for relief as malaria very often presents just like that. Fever on the second day is more likely to be influenza (or another infectious disease) whereas a normal temperature is all the more reason to check on the patient on the third day – when the likelihood of malaria rises exponentially if the fever returns…. As it did in this case.
  • For those of us who operate in a closed community setting - as on a remote site and sometimes in small villages / communities: Beware the “Canteen consultation” - the patient who declares himself fit and looks so at a distance, may still be seriously ill. Only a proper consultation in a clinic setting will reveal a bounding, rapid pulse, actual fever as recorded with a proper thermometer or jaundice observed at close quarters in good light.
  • Although not always typically so, recording a temperature on graph paper remains useful in the detection of a pattern - more so than simple inscriptions in a patient file. Doing so might have revealed a pattern reminiscent of malaria in this patient.
  • Sending a febrile patient out to his room for the night if he had been ‘sleeping’ all day and is still pyrexial can be courting disaster. Cerebral malaria does not always present as full blown ‘coma’ but may have an insidious onset with somnolence and mild cognitive impairment as early ‘soft’ signs.
  • The kidneys are target organs in malaria - a febrile patient with prominent lower back pain and concentrated urine on a remote site in the tropics is a disaster waiting to happen. Ensure adequate hydration - but don’t ‘drown’ the lungs! - And be extremely careful with the use of non-steroidal anti-inflammatories under such conditions. Paracetamol is far safer for the relief of pain and fever and equally effective.
  • Any clinician working in an isolated setting with limited support must use good judgment when it comes to making decisions regarding medical evacuation to a higher level of medical care. It is often better to make use of an opportunity to refer a patient out by ‘routine’ means such as a regular roster charter than to have to become dependent on a dedicated medevac modality by road or air…. Making a call to refer earlier rather than later is often the better decision - as long as the clinician taking care of the patient is assured that he is indeed referring to a higher level of care and not just ‘dumping’ the patient. This sometimes implies that a patient who cannot be taken care of on a remote site will also not be better off in the capital of a developing country but needs to be medevaced all the way to a first class medical facility much further afield. This has several implications including logistics, safety and security issues, cost and time away from site.
    • In this case the clinician on site decided to refer to Dakar but it is the patient who called for referral home. It would have been interesting to see whether the diagnosis of non-falciparum malaria would have been entertained in Dakar…
  • In the absence of a definite diagnosis it is questionable whether it was ethically correct to allow the patient to return to the UK on a commercial airline – the risk to fellow passengers always needs to be considered. In this case the actual cause of the fever turned out to be malaria, which is not contagious in the airline setting. Pragmatism unfortunately often rules in situations like this and in this particular case did not harm any fellow travellers and afforded the patient a rapid, accurate diagnosis once back in the United Kingdom.
  • The UK based doctor acted correctly in immediately asking for a malaria screen as part of the initial work-up of the patient - as much as thirty percent of febrile returned travellers from malaria endemic areas have indeed got some form of malaria. This is more the case in returned VFR’s (Visiting Friends and Relatives) than in expatriates and business travellers but nevertheless should never be omitted in any traveller from a malaria risk area.
  • Typhoid remains part of the differential diagnosis of this patient in spite of the fact that he had been vaccinated against typhoid - the vaccine is only about 75% effective and other Salmonellosis should also be considered. The absence of diarrhoea does not exclude the diagnosis.
  • The use of rapid malaria antigen tests should not just be limited to remote settings far from good laboratory services - they are also useful in a practice that sees febrile returning travellers on a regular basis as it helps in the triage process and to reach a quick decision regarding the likely diagnosis of malaria / not and whether a patient is likely to need urgent admission or not. The clinically very ill patient with a positive rapid test is likely to need immediate admission whereas one that is not acutely ill but still has a positive malaria antigen test would deserve a ‘second look’ regarding his immediate further management. Patients that are not acutely ill, have no obvious other diagnosis and a negative malaria antigen test can be sent home with more confidence than without the test.
  • The use of artemether / lumefantrine in the treatment of P ovale malaria has recently been documented. It is at least as effective as treatment with chloroquine and simplifies decision making in the clinical setting where either ovale, falciparum or a mixed infestation is considered.
  • Clinicians involved in travel health, work across borders and should be au fait with some of the important trade names they are likely to come across - hence the inclusion of the reference to “Riamet®” and “Coartem®” in the case study and highlighting the fact that it is exactly the same drug by a single manufacturer marketed under different trade names. This is sometimes cause for concern amongst travellers and clinicians alike, especially in view of the distrust of medicines in developing countries across the globe and the concern that colleagues in non malaria-endemic countries may “… not know how to treat malaria correctly...”
  • The use of Primaquine to avoid hypnozoite induced relapse is essential not only for the patient but also to ensure that the patient does not perhaps introduce P ovale to the mosquito population on site on his return. (It is not patently clear that he did contract ovale on site - he had been travelling through Dakar and may have been visiting town and villages in the region during his time on the mine.)
    • The argument that he will be returning to an area with P ovale and that he should therefor only receive Primaquine as a radical cure at the end of his contract does not hold true!
  • Finally, it is important for the mine management to know whether there is a real risk for the existence of P ovale malaria on the mine or in its immediate environs as this would influence the way malaria is diagnosed on site and may also have a bearing on the existing malaria vector control programme.
  • Surveillance needs to be set up and an attempt made to identify ovale infested mosquitoes as part of the existing and on-going malaria control programme.
  • The clinicians on site need to consider adding multi-species malaria rapid antigen test kits to their existing side-room laboratory and to institute the use of the kits as part of a suspected malaria management protocol. In the light of just a single case of P ovale being detected in nearly ten years on the project it would not necessarily be wise to replace the single species, P falciparum rapid tests with multi-species tests in the light of the lesser sensitivity and specificity of the latter.
    • Should the mine expand further it may be worthwhile considering a well trained, full time laboratory technician who can do malaria smears on site, but ONLY if a malaria smear quality control programme can be instituted as well.

Plasmodium ovale is seldom diagnosed in returned travellers in South Africa but some cases may be missed either because they are subclinical or because they are reported as P falciparum by less experienced laboratories in non-endemic areas. Treatment with the standard first line regime of artemether / lumefantrine will be effective in warding off the primary attack. Any person who has a relapse soon or weeks after an initial episode of malaria should be considered as perhaps harbouring P ovale or P vivax and a specific attempt made to confirm such as diagnosis to afford the patient a radical cure with Primaquine and avert the possible introduction of P ovale into a previously un-infested community when he returns to the malaria endemic area.

Thank you to everyone who took the time to work through this case study - the author would welcome any constructive remarks and comments.

I would like to thank Prof John Frean, NICD and University of the Witwatersrand for his input on the content of this case.


  1. Plasmodium ovale: PARASITE AND DISEASE. William E Collins, G M Jeffery in CLINICAL MICROBIOLOGY REVIEWS, July 2005, p 570 – 581
  2. Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Dolecek C, Hien TT, do Rosário VE, Arez AP, Pinto J, Michon P, Escalante AA, Nosten F, Burke M, Lee R, Blaze M, Otto TD, Barnwell JW, Pain A, Williams J, White NJ, Day NP, Snounou G, Lockhart PJ, Chiodini PL, Imwong M, Polley SD (2010). "Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally". J Infect Dis 201 (10): 1544–50
  3. http://www.malariasite.com/malaria/africa.htm
  4. The Dielmo Project: A longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am.J.Trop Med. Hyg., 51(2) 1994, pp 123-137. ISSN 0002-9637

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