|Year : 2016 | Volume
| Issue : 2 | Page : 49-57
Blood transfusion malaria: A literature review
Jamilu Abdullahi Faruk
Department of Paediatrics, Ahmadu Bello University, Zaria, Nigeria
|Date of Web Publication||15-May-2017|
Jamilu Abdullahi Faruk
Department of Paediatrics, Ahmadu Bello University, Zaria
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Asymptomatic malaria parasitemia has been documented in donor blood in West Africa. However, donated blood is not routinely screened for malaria parasites (MPs). A literature search was conducted using PubMed and Google Scholar engines, with the search terms “malaria” and “transfusion.” The search results were perused and studies relevant to the subject matter and that available in full text were retrieved. The retrieved studies were then grouped, based on the type of study, into systematic reviews, original articles, and case reports. Commentaries and letters to editors were excluded from the study. Finally, the studies were synthesized based on their themes; detection of MPs in blood donors, studies on MPs in blood recipients, prevention of transfusion-transmitted infections and malaria. In each category, studies from Nigeria and other malaria-endemic African countries were analyzed first, then Asian studies, followed by European and American studies. From the reviewed literature, the overall occurrence of blood transfusion malaria in transfusion recipients is low despite the fact that the potential risk of transmission is quite high as evidenced by the large proportion of blood donors harboring MPs. While several methods are being utilized to reduce the risk of transmission of transfusion malaria, their cost-effectiveness limits wide-range application. However, the riboflavin-ultraviolet light-based parasite reduction system has the potential to revolutionize the incidence of transfusion-transmitted malaria. Therefore, malaria control and eradication interventions need to be strengthened to reduce the rate of infection in the potential blood donors.
Keywords: Malaria, transfusion, transfusion-transmitted
|How to cite this article:|
Faruk JA. Blood transfusion malaria: A literature review. Ann Nigerian Med 2016;10:49-57
| Introduction|| |
Asymptomatic malaria parasitemia has been documented in donor blood in West Africa. However, donated blood is not routinely screened for malaria parasites (MPs) in most malaria-endemic countries unlike what obtains in nonmalaria-endemic regions. The transmission of malaria by blood transfusion was one of the first recorded incidents of transfusion-transmitted infection. As cited by several authors,,,, Gerhardt in 1884 injected two healthy human individuals with blood from patients infected with MPs and demonstrated that malaria could be transmitted by blood inoculation. Malariotherapy was subsequently employed in the treatment of central nervous system syphilis (neurosyphilis)., However, the first case of malaria as an accidental consequence of blood transfusion was described in 1911 by Woolsey as cited by Kitchen and other authors.,, As blood transfusions became widely practiced, observations of accidental transmissions of MPs became increasingly common. According to Bruce-Chwatt, Gordon described the first case of transfusion malaria, following the use of stored blood in 1941.
| Literature Search and Synthesis|| |
A literature search was conducted using PubMed and Google Scholar engines, with the search terms “malaria” and “transfusion”. The search results were perused and studies relevant to the subject matter and that were available in full text were retrieved. The retrieved studies were then grouped, based on the type of study, into systematic reviews, original articles, and case reports. Commentaries and letters to editors were excluded from the study. Finally, the studies were synthesized based on their themes; detection of MPs in blood donors, studies on MPs in blood recipients, prevention of transfusion-transmitted infections and malaria. In each category, studies from malaria-endemic African countries were analyzed first, then Asian studies, followed by nonmalaria-endemic regions.
| Epidemiology of Malaria and Transfusion Malaria|| |
In 2010, 3.3 billion people worldwide were at risk of malaria and an estimated 216 million episodes were recorded. An estimated 655,000 malaria deaths occurred in the same year, the majority of these in Africa and 86% in children under 5 years. Nigeria recorded 3.9 million cases in the same period, with 488,814 malaria deaths. Owing to the increasing reach of core malaria interventions in recent years, these statistics are regularly changing with 584,000 malaria deaths recorded in 2013 and 78% of them in the under-fives.
However, there is a paucity of data on the actual incidence of transfusion malaria, so the total number of cases can only be approximate.,, Most of the available data are from publications of case reports or comprehensive analysis of a series of cases, especially from regions where malaria has been eradicated. In malaria-endemic regions, most of the data obtained are from potential blood donors; therefore, it only measures the potential risk of blood transfusion-induced malaria.,,,,,,,
A systematic review of the relevant literature from Sub-Saharan Africa published in the past three decades found 17 studies. Majority of these studies reviewed were published in or after the year 2000. Nine of the studies were from Nigeria while the other studies were from Benin, Congo, Malawi, Kenya, and Sudan. Two studies were conducted in high malaria transmission season and 13 in both high and low seasons. In the other two studies, the season was not stated. Malaria screening was performed using microscopy in all the studies, except one from Kenya where an automated hematology analyzer, which detects malaria pigment in white blood cells (WBCs), was used. The total number of donated blood units tested for malaria across all the studies was 33,029, with a range of 50–12,375. The median prevalence of asymptomatic parasitemia was 10.2% (range 0.67%–55.0%). Malaria prevalence was higher in the 10 West African studies (median prevalence from Benin and Nigeria, 30.2%) than in the seven studies from all other countries (median prevalence, 6.4%). Only one study established the prevalence of malaria parasitemia in transfusion recipients, with a level of 3.5%.
Since that systematic review, several publications on transfusion malaria have been made, providing more evidence on its incidence, potential risk of transmission, and novel prevention methods.,,,,
Transfusion malaria in endemic countries
In Nigeria, Sodeinde and Dawodu  reported two cases of transfusion malaria. The first was an extremely low birth weight, premature baby who had a blood transfusion on the 7th day of life, and the second case was a term baby with hemolytic anemia due to ABO incompatibility, which required an exchange blood transfusion. Patients manifested new symptoms later, and transfusion malaria was diagnosed. Ibhanesebhor  also found two cases of transfusion-induced malaria among 203 neonates admitted for septicemic illnesses. Sixteen neonates (8%) had MPs without other results to support septicemia and were diagnosed as malaria. Ten of these patients (75%) had congenital malaria, two (13%) had transfusion malaria, and four had neonatal malaria. Ali et al. in Sudan studied 397 children who received blood transfusion, with 6.5% of the blood donors harboring MPs. All the patients were tested for MPs pretransfusion and were negative. Subsequently, patients were retested 4 days after the transfusion, and posttransfusion malaria was diagnosed in 14 (3.5%) of the recipients. Significantly, 12 of the 14 posttransfusion malaria cases were transfused with donor blood containing MPs (true transfusion-induced malaria) while the remaining two cases did not receive blood containing MPs. The implication of these latter two cases is that posttransfusion MPs may not necessarily be transfusion-induced.
The source of posttransfusion MPs has been further elucidated by the studies of Owusu-Ofori et al. and Freimanis et al. Molecular genotyping of parasites showed that the true incidence of transfusion malaria is quite lower than expected. From the study of Owusu-Ofori et al., only one (2%) out of 50, previously MPs negative transfusion recipients, developed parasitemia after the transfusion, which was found to be genotypically identical with that from the blood donor. Six other recipients had MPs posttransfusion who were not identical with the donors' as such could not be termed transfusion-transmitted. The surprise, however, is that of the other 43 (86%) previously MPs negative recipients who received MPs positive blood had no posttransfusion MPs. It is also noteworthy that, unlike the other studies from malaria-endemic regions where the suspected transfusion-malaria cases were symptomatic, the genotypically confirmed transfusion malaria case was asymptomatic. Freimanis et al. used 13 distinct genotypic markers and hence obtained a higher level of posttransfusion parasitemia of 14–28%; however, these were still lower than the MPs positive transfused blood units. In addition, many recipients had MPs before the transfusion. These findings definitely blow wide open the debate on the consequences of transfused parasites in an endemic region.
As reported by Edrissian  in 1974, Iran recorded 111 cases of transfusion malaria from 1963 to 1972. Plasmodium malariae was detected in 73% of the cases and Plasmodium vivax was found in the remaining 27%. The predominance of these species contrasts with most of the West African studies found,,,, where Plasmodium falciparum was universal and probably mirrors the dominant species causing natural infection in the area.
Transfusion malaria in nonendemic countries
Prevalence of transfusion malaria has reduced in Europe since the 1960s. In a case report from the United Kingdom (UK), a 50-year-old male with sickle cell disease and chronic renal failure developed malaria 4 months after receiving a blood transfusion. The blood was traced to a Ghanaian donor. In Switzerland, a 70-year-old male had coronary artery and aortic aneurysm surgery, requiring 26 units of blood products. Two weeks later, he developed a fever and was diagnosed with malaria. One of the blood units used was from a Cameroonian who also had parasitemia; it was established by polymerase chain reaction (PCR) that both donor and patient had identical species of parasite. These are true cases of transfusion malaria as the patients lived in areas where malaria had been eliminated  and patients had never traveled to malaria-endemic areas.
Another study from the UK conducted between 1996 and 1998 reviewed reports of deaths and major complications after blood transfusion. It showed that transfusion-transmitted infections complicated 3% of all blood transfusions in the UK and Ireland, with at least one fatal case of malaria out of 12 such infections. Over a 20-year period, five cases of transfusion malaria were recorded in England as reported by Kitchen.
Transfusion malaria is uncommon in the United States of America (USA). It accounts for 0.2%–0.3% of all cases of malaria  and complicates about three transfusions per year, or only about one case for every 3–4 million units of blood transfused. There are several case reports from the USA and Canada.,,, A retrospective study by Dover et al. in 1971 reported 37 cases in the USA from 1958 to 1971. In that study, 13 out of 21 (61.9%) identified infective donors were servicemen who had recently returned from Vietnam and the plasmodia species of malariae, falciparum, and vivax occurred with the same frequency. In 2001, Mungai et al. reviewed 93 cases of transfusion-transmitted malaria, as reported to the Centers for Disease Control and Prevention, Atlanta, USA, from 1963 to 1999. Transfusion-related malaria had a mortality of 11% in the study, with at least three cases of complicated falciparum infections. Up to 59% of implicated blood donors were foreign born. In Canada, four cases were reported within a 10-year period as compared to 27 cases of bacterial contamination of blood products in the same period.
Potential risk of transfusion-transmitted malaria in endemic countries
Researchers at Ibadan, Nigeria, found MPs among asymptomatic blood donors in 7.8%, 41%, and 19% during 1984, 1991, and 1992, respectively. Malaria antibodies were present in 86% and 100% of these donors from the respective studies., These studies were conducted at different periods of malaria transmission, possibly accounting for the differences. Some researchers from Lagos, Abakaliki, and Nnewi found prevalence of 16.4%, 40.9%, and 30.2%, respectively, with average parasitemias higher in the rainy season compared to the dry season.,, From Jos, the prevalence of asymptomatic parasitemia in blood donors was 11%, while in Zaria, a prevalence of 6.8% was obtained., Overall, there was no definite trend over time demonstrated from these Nigerian studies even though the pattern favored higher parasitemia from the cities in the southern parts (Abakaliki, Nnewi, Lagos, Ibadan) over the northern parts (Jos, Zaria) of the country.
A study by Diop et al. sampled 3001 blood donors across seven blood transfusion centers in Senegal and found malaria antibody prevalence of 65.3%, with 0.53% positive for Plasmodium lactate dehydrogenase (LDH) antigen. Asymptomatic carriage of Plasmodium was more common during the rainy season and in individuals with high frequency of malaria attacks in the past, especially if the last episode was not treated. In Ethiopia, a study of 600 blood donors carried out across four blood banks detected asymptomatic parasitemia in only 1% of donors. Furthermore, 493 blood donors from two blood banks in the city of Yaoundé, Cameroon, were tested for MPs. Asymptomatic parasitemia was found in 6.3% of them, with P. falciparum detected in 90.3% of those having MPs and P. malariae in the remaining 9.7%. These different prevalence rates may just be as a result of the timing of the studies and seasonal variation of malaria infection, rather than a regional variation in the distribution of the disease. The sensitivity of the antigen-based tests may also affect the reported values. Antibody-based tests, however, tend to overestimate the risk evidenced by the disparity within studies that utilized both methods.,,,
One subtle finding from the malaria-endemic regions is that often the prevalence of MPs in the recipients of blood transfusion is quite high before receiving the transfusion, with several studies showing similar prevalence of parasitemia between donors and pretransfusion recipients., Indeed, studies of children requiring blood transfusion, not looking out for donor MPs, have established very high pretransfusion MPs prevalence of 76% and 83% in Uganda and Nigeria, respectively.,,
Risk factors of transfusion-transmitted malaria in nonendemic countries
The risk of transfusion malaria in nonmalaria-endemic countries is principally contributed by blood donors previously living or haven traveled to malaria-endemic countries., Donors may remain infective for up to 5 years with P. falciparum and P. vivax, 7 years with Plasmodium ovale, and 46 years with P. malariae since the travel to the malaria-endemic area., Mixed infections, with more than one Plasmodium species, are not uncommon. In addition, all the donors were asymptomatic. Surprisingly, about 3.78% of donors living in a nonendemic area, without history of exposure to malaria, turned out to be positive for malaria deoxyribonucleic acid (DNA).
| Transmission of Malaria Parasites|| |
Infective female Anopheles mosquitoes inject malaria sporozoites into a susceptible host during a blood meal. Malaria can also be acquired as a congenital infection via vertical transmission across the placenta from an infected pregnant woman to the fetus.,,
In transfusion-induced malaria, parasites are capable of being transmitted through the blood by virtue of the persistence of trophozoites and merozoites in the bloodstream of carriers, their potential viability in stored blood, and the prevalence of the parasite in the donor community.,,P. falciparum has been shown to persist in blood stored at 4°C for 28 days although it loses its ability to multiply after 14 days of storage. Furthermore, because the infecting parasites are erythrocytic forms (not sporozoites), no exoerythrocytic cycle will be established and so vivax and ovale malaria will not relapse.
Blood transmission of MPs is commonly associated with red blood cell (RBC) concentrates but has also been reported in components such as platelets and frozen plasma.,, Therefore, nearly all blood components can transmit malaria.
| Clinical Manifestations of Transfusion Malaria|| |
The incubation period of vector-transmitted malaria varies from 10 to 20 days depending on the species. Theoretically, in transfusion-transmitted malaria, parasitemia should be detectable immediately, and hence, the incubation period should be shorter than with mosquito-transmitted malaria. However, reported incubation periods have been as short as 1–3 days , as there is no exoerythrocytic phase;,, however, it has also taken up to 4 months in others. The variations noted may depend on the number and species of parasites transfused or the susceptibility of the recipient to malaria. These factors will influence the time needed to build up parasitemia sufficient to cause symptoms.,, All species of Plasmodium causing human malaria have been implicated in transfusion-related transmission in various proportions.,,,
In malaria-endemic countries, manifestations of blood transfusion malaria are similar to that of the natural infection ,, although, in research situations, posttransfusion MPs have been detected before the recipients developed any symptom., On the other hand, only a small portion of posttransfusion fevers has been confirmed to have MPs. In nonendemic countries, severe forms of malaria have been observed,, including multiple organ failure with a fatal outcome ,, and cerebral malaria.
| Diagnosis of Transfusion Malaria|| |
A high index of suspicion is required to investigate any fever developing after blood transfusion, for potential malaria. The mean interval between blood transfusion and clinical/laboratory diagnosis of malaria was 3 days in one study  but may take 1–6 months, especially in nonmalaria-endemic regions.
Microscopic examination of stained blood smears remains the “gold standard” for detection of malaria parasitemia,, with detection of as low as 5–10 parasites/μl of blood., Antigen detection tests were developed as a means of simple, quick, accurate, and cost-effective diagnosis of malaria parasitemia. These rapid diagnostic tests (RDTs) detect P. falciparum-specific histidine-rich protein II (HRPII) and parasite-specific LDH and can distinguish non-falciparum infections from mixed infections.,, Positive HRPII-based test results persist for some time after effective treatment and may lead to a false positive diagnosis although both tests have very high sensitivity and specificity.,
Levels of parasitemia may be too low to detect by RDTs or microscopy, but PCR can be 100-fold more sensitive than either when appropriate primers are used. PCR detects Plasmodium DNA or ribonucleic acid  and has proved vital in distinguishing transfusion-transmitted malaria from posttransfusion malaria through identification of parasitic allelic genes., Serological tests, based on detection of antibodies against asexual blood stage MPs, such as the immunofluorescent antibody testing (IFA), are useful in epidemiological surveys, for screening potential donors. IFA is highly sensitive and specific although it is time-consuming and subjective since it does not necessarily indicate a recent infection., Enzyme immunoassays have proved to be very sensitive.In vitro cultures of MPs have also been employed for research purposes.
Combinations of these diagnostic tests have been utilized in several settings, and coupled with prudent selection criteria, these combinations could be cost-effective on the long run.,, The value of molecular genotypic testing cannot be overemphasized, however, especially in malaria-endemic countries, where it is least likely to be in routine use.
| Treatment of Transfusion Malaria|| |
Antimalarial combination therapy is now recommended by the WHO for the treatment of uncomplicated falciparum malaria to counter the threat of resistance associated with monotherapies. This means the simultaneous use of two or more blood schizonticidal drugs with independent modes of action and thus unrelated biochemical targets in the parasite. Thus, artemisinin-based combination therapies (ACTs) are currently the first-line treatment for uncomplicated falciparum malaria. For severe malaria, the two classes of drugs currently available for parenteral treatment are the cinchona alkaloids (quinine and quinidine) and the artemisinin monotherapies (artesunate, artemether, and artemotil).
Chloroquine was used successfully to treat blood transfusion-induced malaria in the pre-ACTs era,,, and since there is no exoerythrocytic phase, tissue schizonticides such as primaquine are unnecessary.,, One case however required additional treatment with sulfadoxine-pyrimethamine and doxycycline before clearance of parasitemia and relief of symptoms, and another patient was given primaquine.
| Prevention of Transfusion Malaria in Endemic Countries|| |
Transfusion-transmitted diseases are directly proportionate to the prevalence of the infection in the blood donor community. Thus, the risk of transfusion malaria is high in all malaria-endemic areas. The primary prevention of blood transfusion-induced malaria is, therefore, to eradicate or control malaria in the general population by preventive treatment in high-risk groups and vector control through the use of insecticide-treated nets and indoor residual spraying.
Secondary prevention of blood transfusion-induced malaria depends on screening and deferring from donation, of possibly infected blood donors, elimination of actual or possible plasmodial infection in the donor and the recipient of the blood. These measures however are employed to different extents in malaria endemic. Donor deferral based on history of exposure to malaria is not feasible in endemic countries as the exposure is universal. Therefore, parasite detection may be more appropriate. Despite the perceived low sensitivity of microscopic examination and RDTs in detecting low-level asymptomatic parasitemia,,, these methods have been used widely to report the very high parasitemia levels from malaria-endemic countries., Antibody detection tests are of limited value in endemic regions. PCR, on the other hand, has a huge role to play in precisely defining transfusion malaria but is seldom available. These reasons therefore make the elimination of parasites, the better option in endemic areas. Thus, the judicious use of antimalarial drugs has been suggested as a necessity either in the donor before blood donation  or in the recipient. The prophylactic treatment of the recipient is thought to be more reliable and easier although its practice varies from place to place.,,, In a Chinese study, recipients given quinine for 3 days after the transfusion had no attacks of malaria while one-half of those who received no medication developed the infection within 3 weeks. Obviously, this strategy is shrouded in an ethical dilemma of knowingly transfusing a potentially lethal infectious agent to a recipient, in an attempt to give another potentially beneficial therapy.
Another approach to the prevention of transfusion-associated malaria involves destruction of the parasites in the blood bag. Photochemical treatment with amotosalen and long wavelength ultraviolet (UV) light has been shown to be effective against viruses, bacteria, and protozoa, including P. falciparum. This could reduce the risk of transfusion-transmitted infections and avoid unnecessary donor exclusions and wastage of blood products.,, There has been tremendous success in that regard in the past few years. Chaar et al. conducted in vitro studies on whole blood that was inoculated with MPs and treated with riboflavin and then irradiated with UV rays. Parasite integrity and viability were disrupted, with subsequent reduction of polymerase-dependent amplification by 99%. There was no significant hemolysis to the red cells also. Then, they came the randomized controlled double-blinded clinical trial, of the whole blood pathogen reduction system, which was designed to destroy MPs and inactivate leukocytes. The trials were conducted in Ghana, whereby patients were randomized to receive whole blood that was treated or untreated with the riboflavin-UV light-based system. The results revealed a marked reduction in posttransfusion MPs detected via PCR, in the treated group, compared to the untreated group, with a high statistical significance. Only 4% of the treated group had transfusion-transmitted MPs, in contrast to 22% of the untreated group. The efficacy and safety profile of the transfusion were similar across both groups. If this parasite reduction system proves to be cost-effective, then it will revolutionize the outcome of transfusion-transmitted MPs in endemic regions.
Prevention of transfusion-transmitted malaria in nonendemic countries
The risk of transfusion-induced malaria in nonendemic areas is introduced from either travelers to or immigrants from malaria-endemic areas.,, The current strategies thus are based on risk group assessment and include donor deferral combined with other measures such as parasite detection and inactivation.,, Donor deferral is based on exclusion from donation for 3 years, of all persons having symptoms of malaria, or who lived in an endemic area, or who traveled to an endemic country in the preceding 3 years from the intended day of blood donation.,, This policy has maintained risk of transfusion malaria at low levels , but does not eliminate the risk and needs to be supported by parasite detection methods., Combination of microscopy and RDTs has proved very effective in some nonendemic areas, and when used in conjunction with donor deferral, it has maintained transfusion malaria at zero in these regions. PCR is routinely utilized and may prove more cost-effective when combined with donor deferral as it avoids unnecessary blood donor loss. Serological test by the use of the IFA technique is most widely used.,,, This is used in combination with the donor deferral system. A positive test signifies only previous infection, either recent or distant and not the actual presence of MPs, but a negative test indicates either a complete cure or an absence of previous infection. The IFA may therefore result in the exclusion of some potential donors since the presence of antibodies does not necessarily indicate the presence of parasitemia.,,
Leukoreduction filters have been used to reduce transmission of viral organisms such as Cytomegalovirus and human T-lymphotropic virus Type I and other organisms which exist intracellularly within WBCs. An unexplained decrease in the incidence of transfusion-transmitted malaria was noticed in recent years, paralleling the increasing use of leukoreduction filters. Malaria-infected RBCs have been shown to adhere directly to filter fibers, adhere to other RBCs (rouleaux formation), or adhere to platelets which were adherent to the filter fibers. The efficiency of this removal however requires further study. With the advent of the parasite reduction systems, this will further improve the safety of the blood supply system.,,
Screening and excluding donors waste up to 5%–6.5% of blood donations , although this may be more than 30% in some areas if all malaria-infected blood is rejected. However, the cost per case of malaria prevented is higher if recipient antimalarials are used, especially with the new ACTs. The cost of avoiding an infection cannot be estimated, but it is certain to be enormous. This has led to rising costs of blood components and associated services with marginal increase in safety.
| Conclusion|| |
Blood transfusion-induced malaria has been recognized for centuries, and although malaria infection has been eliminated in many regions of the world, blood transfusion remains a potential source of parasite introduction to these areas and may also be a significant cause of morbidity in the hitherto malaria-endemic areas. Although there are several methods of preventing transfusion malaria, their cost-effectiveness is still not very clear. On the other hand, there is a high prevalence of asymptomatic parasitemia among blood donors in malaria-endemic regions, but strategies to curtail its transmission are seldom applied. The advent of the riboflavin-UV light parasite reduction system has the potential to eradicate blood transfusion malaria.
I wish to express my profound and sincere gratitude to Professor G. O Ogunrinde and Professor Aisha I. Mamman for their time, guidance, and mentoring while writing this literature review. I would also like to express my appreciation to the Head, Department of Paediatrics, ABUTH, for the support and direction given to me during this work. To all my teachers, seniors, and other colleagues, I would like to thank them for all the critiques and comments passed, leading up to the completion of the study.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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