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  • Open Access

A systematic review of transfusion-transmitted malaria in non-endemic areas

Contributed equally
Malaria Journal201817:36

https://doi.org/10.1186/s12936-018-2181-0

  • Received: 20 July 2017
  • Accepted: 10 January 2018
  • Published:

Abstract

Background

Transfusion-transmitted malaria (TTM) is an accidental Plasmodium infection caused by whole blood or a blood component transfusion from a malaria infected donor to a recipient. Infected blood transfusions directly release malaria parasites in the recipient’s bloodstream triggering the development of high risk complications, and potentially leading to a fatal outcome especially in individuals with no previous exposure to malaria or in immuno-compromised patients. A systematic review was conducted on TTM case reports in non-endemic areas to describe the epidemiological characteristics of blood donors and recipients.

Methods

Relevant articles were retrieved from Pubmed, EMBASE, Scopus, and LILACS. From each selected study the following data were extracted: study area, gender and age of blood donor and recipient, blood component associated with TTM, Plasmodium species, malaria diagnostic method employed, blood donor screening method, incubation period between the infected transfusion and the onset of clinical symptoms in the recipient, time elapsed between the clinical symptoms and the diagnosis of malaria, infection outcome, country of origin of the blood donor and time of the last potential malaria exposure.

Results

Plasmodium species were detected in 100 TTM case reports with a different frequency: 45% Plasmodium falciparum, 30% Plasmodium malariae, 16% Plasmodium vivax, 4% Plasmodium ovale, 2% Plasmodium knowlesi, 1% mixed infection P. falciparum/P. malariae. The majority of fatal outcomes (11/45) was caused by P. falciparum whilst the other fatalities occurred in individuals infected by P. malariae (2/30) and P. ovale (1/4). However, non P. falciparum fatalities were not attributed directly to malaria. The incubation time for all Plasmodium species TTM case reports was longer than what expected in natural infections. This difference was statistically significant for P. malariae (p = 0.006). A longer incubation time in the recipient together with a chronic infection at low parasite density of the donor makes P. malariae a subtle but not negligible risk for blood safety aside from P. falciparum.

Conclusions

TTM risk needs to be taken into account in order to enhance the safety of the blood supply chain from donors to recipients by means of appropriate diagnostic tools.

Keywords

  • Blood transfusion
  • Malaria
  • Plasmodium
  • Blood component transfusion
  • Transfusion-transmitted malaria (TTM)

Background

Malaria is an infectious disease caused by intracellular protozoan parasites of the genus Plasmodium responsible for a potentially fatal acute febrile illness following invasion and multiplication in human red blood cells (RBCs) during their complex life cycle. Five species of Plasmodium are currently known to cause malaria in humans: the deadliest Plasmodium falciparum and Plasmodium vivax, Plasmodium malariae, Plasmodium ovale, Plasmodium knowlesi. Malaria parasites are naturally transmitted by the infective bites of female Anopheles mosquitoes during their blood meal. Malaria can manifest with severe symptoms leading to a fatal outcome in non-immune individuals, often young children and pregnant women in endemic areas or naïve adults in non-endemic settings, and remains asymptomatic in adults who have acquired a premunition maintained by repeated antigen exposure.

Transfusion-transmitted malaria (TTM) is an accidental Plasmodium infection caused by the transfusion of whole blood or a blood component from a malaria infected donor to a recipient, described for the first time by Woolsey in 1911 [1], that may cause severe clinical symptoms in the recipients, especially in those with no previous exposure to malaria or in immuno-compromised patients due to other coexisting diseases. Several systematic reviews have addressed the knowledge gap still existing in the epidemiology of TTM in the United States [2], Canada [3] and the Americas [4].

Plasmodium falciparum, P. vivax and P. malariae are the species most frequently detected in TTM [5]. Various aspects of the parasite biology make this accidental route of infection feasible such as the persistence of infection: P. falciparum can persist for at least 1 year before being cleared, P. vivax for 3 years whereas P. malariae is known to remain as a chronic infection at low density for decades [6]. All Plasmodium species are able to survive in stored blood, even if frozen, and retain their viability for at least 1 week, possibly well over 10 days depending on the conditions of storage; in fact, microscopically detectable malaria parasites were present even after 28 days of storage at 4 °C although a decrease of infectivity after 2 weeks was observed [6, 7]. An important difference between the natural infection and TTM is that the former undergoes an initial asymptomatic phase (pre-erythrocytic) which allows the activation of innate immunity cells against malaria parasites. This early phase has advantages on both sides of the host parasite arms race: the innate immunity gives the naïve host time to develop a more specific protective immunity; meanwhile the parasites manipulate the host’s immune system in order to escape. Infected blood transfusions directly release malaria parasites in the recipient’s bloodstream triggering the development of high risk complications and potentially leading to a fatal outcome [8]. Experimental evidence suggests that as few as 10 infected RBCs can be sufficient to transmit the infection; thus, even a small inoculum is potentially infectious. However, the mean incubation period for TTM is generally longer than the mean incubation period for the mosquito-transmitted malaria (MTM) for all Plasmodium species as reported by [9]: 16.0 (8–29) days for P. falciparum TTM compared to 13.1 (7–27) days in P. falciparum MTM; 57. 2 (6–106) days for P. malariae TTM compared to 34.8 (27–37) days for P. malariae MTM; 19.6 (8–30) days for P. vivax TTM compared to 13.4 (8–31) days for P. vivax MTM; 23 days for P. ovale TTM compared to 13.6 (11–16) days for P. ovale MTM [9]. Blood components such as RBCs, platelets and plasma, are commonly transfused to treat various conditions ranging from surgical procedures causing a temporary anaemia to a chronic one due to haematological disorders (haemoglobinopathies, glucose-6-phosphate-dehydrogenase (G6PD) deficiency, haemophilia). Blood banks require a preliminary screening of a potential blood donor to exclude the risk of current or previous infections which can be transmitted by a blood transfusion, including malaria. Criteria for haemovigilance are defined by the World Health Organization (WHO) and are adapted to each country according to national guidelines. Some countries such as USA rely on a pre-donation questionnaire for the screening of potential infected donors whereas some others, including France, UK and Australia, use antibody testing on donors who are considered at risk on the basis of the preliminary questionnaire [3]. Appropriate diagnostic tools need to be employed in order to enhance the safety of the blood supply chain from donors to recipients tailored to the local TTM risk. The sensitivity and specificity of the screening strategy of blood donors remains the crucial issue in order to ensure the safety of blood transfusions particularly in the case of malaria: in fact, serological tests currently employed do not indicate the actual parasitaemia because antibody levels can remain elevated for many years after infection of P. falciparum and P. vivax [10]. Also, the initial clinical symptoms are generally aspecific making the diagnosis more difficult and resulting in a further delay. Delayed or missed diagnosis of P. falciparum in particular increases the risk of severe disease which may be fatal especially in non-immune individuals.

Furthermore new technologies are available to selectively inactivate pathogens without damaging cells or plasma; a combination of riboflavin as a photosensitizer with a UV light illumination device (Mirasol System for Whole Blood; Terumo BCT, Lakewood, Colo.) proved to substantially reduce P. falciparum infectivity in whole blood samples without altering cell quality parameters [11]; this inactivation technology may well represent another layer of control to reduce the risk of TTM.

Lastly, infected recipients who do not develop any clinical illness may become asymptomatic carriers and thus a reservoir of malaria parasites if competent vectors were to be present; this event has serious implications especially in non-endemic countries where the majority of the population has never been exposed to malaria parasites.

The primary objective of this systematic review was to describe the epidemiological characteristics of TTM in non-endemic countries based on data available in the literature in order to evaluate the extent and dynamics of this particular risk of malaria transmission. The review specifically investigated: (i) which Plasmodium species are more often detected in TTM; (ii) if other Plasmodium species besides P. falciparum are likely to cause a lethal outcome of TTM; (iii) whether the incubation time in TTM is longer than in the natural infection; (iv) which blood component is more likely to be infective for the recipient (whole blood, red blood cells, platelets or plasma); (v) which diagnostic methods were used in donor screening and recipient diagnosis (microscopy, serological or molecular tests).

Methods

Literature search

A systematic review of all articles on TTM in non-endemic areas was carried out. Relevant articles were retrieved from Pubmed, EMBASE, Scopus, and LILACS databases using combinations of the following search terms: “malaria”, “blood transfusion”, “Plasmodium”, “transfusion”, adapted to each database without date or language restrictions until May 17th 2017. TTM cases in USA were retrieved from the annual Morbidity and Mortality Weekly Reports (MMWR) malaria surveillance reports. The following combination of MeSH and free string terms were used specifically in Pubmed:

((“Platelet Transfusion”[MeSH] OR “Transfusion Medicine”[MeSH] OR “Lymphocyte Transfusion”[MeSH] OR “Leukocyte Transfusion”[MeSH] OR “Erythrocyte Transfusion”[MeSH] OR “Blood Component Transfusion”[MeSH]) OR (Transfusion*)) AND ((malaria*) OR (Plasmodi*) OR (malaria [MeSH])). Original research papers were included and additional references retrieved from narrative reviews; restriction to case reports was deemed necessary as the main scope of this systematic review was to investigate in fine details the relevant characteristics of each reported case of TTM. Two independent investigators (FV, EM) screened titles and abstracts, selected articles for full text review, performed the final article selection; a third reviewer (AA) was consulted in case of disagreement in order to reach a consensus. Case reports were excluded if the Plasmodium species was described as “tertian” without further identification. Also, case reports occurred in malaria endemic countries were not considered unless the case report was ascertained to have happened in a non-endemic area of the country. Articles in Chinese, Russian, Arabic and Turkish languages without at least a summary in English were dropped. From each study the following data was extracted: study area, gender and age of blood donor and recipient, blood component transfused, Plasmodium species, malaria diagnostic method employed, blood donor screening method, incubation period (i.e. the time elapsed between the infected transfusion and the onset of clinical symptoms in the recipient), delayed diagnosis (i.e. time elapsed between the onset of clinical symptoms and the diagnosis of malaria), infection outcome, country of origin of the blood donor and time of the last potential malaria exposure. The protocol for this systematic review was published on PROSPERO database with the registration number CRD 42017062298.

Statistical analysis

The incubation time of each TTM case report was analysed through standard one sample two-tailed t-tests (level of significance α = 0.05) to evaluate the difference between incubation periods of TTM and MTM for each Plasmodium species. Reference mean values of MTM were drawn from the results shown by Dover and Schultz [9]. All statistical analyses were performed using R software, version 3.3.3 [12].

Results

The number of selected papers at each step of the screening and criteria for exclusion/inclusion are reported in the flow diagram (Fig. 1); 100 case reports of TTM were retrieved for the purpose of this review and the main epidemiological data is provided by Table 1. Fifty-four of these case reports occurred in the American continent, 38 in Europe, 3 in the Mediterranean area, 1 in India, 4 in South-East Asia.
Fig. 1
Fig. 1

Flow diagram of the articles selection on transfusion transmitted- malaria in non-endemic areas

Table 1

Reported cases of transfusion- transmitted malaria (TTM) in malaria non-endemic areas

Countrya

Year

Donor gender and age

Donor origin and last exposure

Recipient gender and age

Recipient incubation (delayed diagnosis)

Recipient outcome

Blood component transfused

Plasmodium species

Diagnosis method recipient (donor)

References

Canada

Western region

1936

M

Mediterranean area

F

13 years

3 weeks (5 weeks)

Recovery

WB

P. malariae

LM (LM)

[17]

Ontario

1936

M

Romania

25 years

F

26 days (2 weeks)

Recovery

WB

P. malariae

LM (LM)

[18]

Alberta

1977

F

23 years

Africa

2 years

F

60 years

29 days (29 days)

Recovery

WB

P. ovale

LM (IFAT)

[19]

Quebec

1994

N/A

Cameroon

> 3 years

M

63 years

N/A (3 weeks)

Recovery

RBCs, PLTs, FFP

P. falciparum

LM (LM)

[20]

Ontario

1995

M

Mali

4 years

F

24 years

15 days (3 days)

Recovery

RBCs

P. falciparum

LM, PCR (PCR)

[20]

Ontario

1997

F

19 years

Ghana

4 years

F

62 years

21 days (5 weeks)

Recovery

RBCs, FFP

P. falciparum

LM, PCR

[20]

USA

New York

1911

N/A

N/A

M

54 years

11 days

“Pernicious anaemia”

WB

P. vivax

LM

[1]

Colorado

1929

M

32 years

Greece

16 years

F

2½ years

19–25 days (on the day)

Recovery

WB

P. malariae

LM (LM)

[21]

New York

1932

M

Italy

F

1.5 years

4 weeks (17 days)

Recovery

WB

P. malariae

LM

[22]

New York

1932

M

Italy

12 years

M

9 months

6 weeks

Recovery

WB

P. malariae

LM

[22]

New York

1933

F

Greece

F

8 years

< 8 weeks

Death due to pneumonia

WB

P. malariae

LM

[22]

New York

1936

M

Greece

33 years

F

1 year

29 days

Recovery

WB

P. malariae

LM

[22]

New York

1936

M

Colombia

10 years

M

3 years

2 months

Recovery

WB

P. malariae

LM

[22]

New York

1944

M

40 years

North Africa veteran

1 year

F

32 years

11–4 days (35 days)

Recovery

WB

P. malariae

LM (LM)

[23]

Rhode Island

1946

M or F

Italy or New England

F

40 years

2 months (2 days)

Recovery

WB, FFP

P. malariae

LM (LM)

[24]

Pennsylvania

1946

N/A

Army returnee

F

3 weeks (9 days)

Recovery

WB

P. vivax

LM

[25]

California

1968

M

19 years

Vietnam veteran

7 months

M

60 years

4 days (on the day)

N/A

WB

P. falciparum

LM (LM)

[26]

Connecticut

1968

N/A

Mexico

5 years

F

8 months

6 ½ months

Recovery

WB

P. malariae

LM

[27]

Washington state

1968

M

22 years

Vietnam veteran

1 year

F

54 years

13 days (9 days)

Recovery

WB

P. falciparum

LM (LM, IFAT)

[28]

Oklahoma

1968

M

21 years

Vietnam veteran

5 months

F

25 years

16 days (7 days)

Recovery

WB

P. falciparum

LM (LM)

[28]

Washington D.C.

1969

M

Nigeria

> 2 years

M

56 years

17 days (6 days)

Death

WB

P. falciparum

LM (LM, IFAT)

[29]

New York

1970

M

Ghana

1 year

M

34 years

6 days (2 days)

Recovery

WB

P. falciparum

LM (LM, IFAT)

[30]

Chicago

1972

N/A

N/A

M

5 months

16 days (6 days)

Recovery

WB

P. vivax

LM

[31]

New York

1971

N/A

N/A

M

24 years

Multiple transfusions (7 days)

Recovery

WB

P. vivax

LM (IFAT)

[32]

New York

1974

N/A

N/A

F

42 years

9 weeks (on the day)

Recovery

RBCs, PLTs, FFP

P. malariae

LM (IFAT)

[32]

New York

1974

F

53 years

Greece

22 years

F

78 years

Multiple transfusions (~ 30 days)

Recovery

WB, RBCs

P. malariae

LM, IFAT (IFAT)

[33]

New York

1974

M

38 years

Cyprus

4 years

F

42 years

35 days (1 month)

Recovery

RBCs, PLTs, FFP

P. malariae

LM, IFAT (IFAT)

[33]

Tennessee

1974

M

28 years

Nigeria

8 years

F

15 years

3 months (12 days)

Recovery

WB

P. malariae

LM (LM, IFAT)

[34]

Wisconsin

1977

N/A

Africa

recent

F

57 years

Multiple transfusions (28 days)

Death due to refractory leukaemia

PLTs

P. falciparum

LM (LM)

[35]

New York state

1978

M

Ghana

10 months

F

65 years

16 days (1 day)

Recovery

WB, RBCs, FFP

P. falciparum

LM (IFAT)

[36]

California

1980

M

N/A

M

6 years

15 days (2 days)

Recovery

RBCs

P. falciparum

LM (LM)

[37]

California

1982

M

Nigeria

7 years

M

premature

6 weeks

Death due to pneumonia

WB

P. ovale

LM, IFAT (IFAT)

[38]

Boston

1982

N/A

N/A

M

premature

7 weeks (on the day)

Recovery

RBCs

P. malariae

LM (LM)

[39]

Boston

1982

N/A

N/A

M

premature

10 weeks (on the day)

Recovery

RBCs

P. malariae

LM (LM)

[39]

California

1983

M

Guatemala

6 months

M

premature

5 weeks (on the day)

Recovery

WB

P. vivax

LM (LM)

[40]

California

1983

M

South America

6 months

M

infant

14 days (on the day)

Recovery

WB

P. vivax

LM (IFAT)

[40]

Texas

1992

M

19 years

Nigeria

7 months

F

71 years

7 days (on the day)

N/A

RBCs, PLTs

P. falciparum

LM (IFAT)

[41]

Texas

1992

M

19 years

Nigeria

7 months

M

65 years

N/A

N/A

RBCs

P. falciparum

LM (IFAT)

[41]

California

1992

M

55 years

China

44 years

M

44 years

7 months (3 months)

Recovery

RBCs

P. malariae

LM (IFAT)

[41]

Texas

1994

M

Nigeria recent

F

59 years

20 days (on the day)

Recovery

RBCs

P. falciparum

LM (LM, IFAT)

[42]

 Texas

1994

M

Ghana recent

M

46 years

16 days (7 days)

Recovery

RBCs, FFP

P. falciparum

LM (LM, IFAT)

[42]

Pennsylvania

1995

M

Nigeria

3 years

F

72 years

Multiple transfusions

Recovery

RBCs

P. falciparum

LM (LM, IFAT)

[43]

Missouri

1996

M

West Africa

1 year

M

70 years

15 days (on the day)

Death

RBCs

P. falciparum

LM (LM, IFAT, PCR)

[44]

Missouri

1997

M

West Africa

2 years

M

85 years

21 days (on the day)

Death

RBCs

P. falciparum

LM (LM, IFAT, PCR)

[44]

Pennsylvania

1998

M

West Africa

2 years

M

49 years

35 days (on the day)

Recovery

RBCs

P. falciparum

LM (IFAT, PCR)

[44]

Texas

2003

M

Ghana

2 years

69 years

17 days (3 days)

Recovery

RBCs

P. falciparum

LM (LM, PCR, IFAT)

[45]

Texas

2007

M

Nigeria

6 years

F

25 years

Multiple transfusions

Recovery

RBCs

P. falciparum

LM (IFAT)

[46]

Washington D.C.

2007

M

West Africa

F

15 days (on the day)

Recovery

RBCs

P. falciparum

LM, PCR (LM)

[47]

Washington D.C.

2007

M

27 years

Nigeria

3 years

M

27 years

13–28 days (11 days)

Recovery

RBCs

P. falciparum

LM (IFAT, PCR)

[47]

New Jersey

2007

F

30 years

Uganda

> 1 year

M

78 years

1 year

Recovery

RBCs

P. falciparum

LM (IFAT, PCR)

[47]

N/A

2007

M

21 years

Benin

4 years

F

55 years

1 month

Recovery

RBCs, PLTs, FFP

P. falciparum

LM, IFAT, PCR (IFAT, EIA)

[48]

Georgia

2015

M

20 years

Liberia

15 years

M

76 years

6 months (2 days)

Recovery

RBCs, FFP

P. malariae

LM, PCR (LM, PCR, ELISA)

[49]

Colombia

Cali

2011

N/A

Rural area

9 months

F

Premature

Multiple transfusions (on the day)

Recovery

RBCs

P. vivax

LM (PCR)

[50]

Brasil

 Sao Paulo

2008

M

Atlantic forest

1 year

N/A

75 days (on the day)

Recovery

RBCs, PLTs, FFP

P. malariae

LM (LM, PCR, IFAT)

[51]

Spain

Valencia

1987

N/A

Congo

F

32years

7 days (on the day)

N/A

WB

P. falciparum

LM (IFAT)

[52]

Madrid

1997

N/A

Central Africa

F

63 years

3 weeks (4 weeks)

N/A

WB

P. falciparum

LM (IFAT)

[53]

Cordoba

2002

N/A

N/A

F

26 years

Multiple transfusions (128 days)

Recovery

WB, RBCs

P. falciparum

LM

IFAT

[54]

UK

Midlands

1935

M

India

2 years

M

26 years

19 days (5 days)

Recovery

WB

P. vivax

LM (LM)

[55]

London

1938

M

Ceylon

12 years

F

3 months

10 weeks (on the day)

Death

WB

P. malariae

LM (LM)

[56]

Durham

1946

M

Yemen

7 years

F

18 years

7–8 weeks (10 days)

Recovery

WB

P. malariae

LM (LM)

[57]

N/A

1959

M

19 years

Nigeria

1 year

F

41 years

16 days (6 days)

Recovery

WB

P. falciparum

LM (LM)

[58]

Oxford

1966

M

Far East

20 years

M

33 years

10 weeks (1 day)

Recovery

WB, FFP

P. malariae

LM (LM)

[59]

Buckingmanshire

1967

M

Army returnee

M

51 years

N/A

Recovery

FFP

P. malariae

LM (LM)

[60]

Buckingmanshire

1968

M

Africa

18 months

M

49 years

11 days (12 days)

Recovery

WB

P. falciparum

LM (LM, IFAT)

[60]

London

1986

M

Africa

F

72 years

13 days (12 days)

N/A

PLTs

P. falciparum

LM (LM, IFAT)

[61]

London

1986

M

Ghana

F

81 years

14 days

N/A

WB

P. falciparum

LM (IFAT)

[61]

N/A

1994

F

Ghana

1 year

M

15 days (on the day)

N/A

WB

P. falciparum

LM (EIA, IFAT)

[5]

N/A

1997

F

19 years

Ghana

3 years

M

62 years

4 days

Death

WB

P. falciparum

(EIA, IFAT)

[5]

N/A

2003

F

38 years

Ghana

7 years

M

51 years

N/A

Death

WB

P. falciparum

LM (EIA, IFAT)

[5]

Netherlands

Leiden

2011

M

36 years

Africa

Costa Rica

> 4 years

F

59 years

2 months (on the day)

Recovery

RBCs

P. malariae

LM, PCR (LM, IFAT, PCR)

[62]

Germany

Göttingen

1998

N/A

N/A

M

18 months

14 days (9 days)

Recovery

RBCs

P. falciparum

LM

[63]

France

Poitiers

1969

M

Portugal

5 months

F

15 days

(1 month)

Recovery

WB

P. malariae

LM (IFAT)

[64]

Paris

1957

F

Tunisia

27 years

F

32 years

48 days (4 days)

Recovery

WB

P. vivax

LM

[65]

Paris

1973

M

Senegal

13 years

M

30 years

14 days (9 days)

Recovery

WB

P. falciparum

LM (IFAT)

[65]

Paris

1975

N/A

N/A

F

24 years

15 days (18 days)

Recovery

WB

Plasmodium

LM (IFAT)

[66]

Tours

1977

N/A

N/A

F

47 years

15 days (on the day)

Recovery

WB

P. vivax

LM

[67]

Rouen

1976

N/A

Senegal

N/A

12 days (10 days)

Death

N/A

P. falciparum

(IFAT)

[68]

Rouen

1976

N/A

Ivory Coast

N/A

13 days (6 days)

Death

N/A

P. falciparum

(IFAT)

[68]

Rouen

1978

N/A

N/A

N/A

60 days (2 days)

Recovery

N/A

P. malariae

(IFAT)

[68]

Nancy

1979

M

Zaire

1 month

F

29 years

15 days (43 days)

Recovery

RBCs

P. falciparum

P. malariae

LM (IFAT)

[69]

Crèteil

1980

M

Central Africa

M

infant

2 months (3 days)

Recovery

RBCs, FFP

P. malariae

LM

[70]

Aulnay-sous-Bois

1986

N/A

N/A

F

64 years

16 days (on the day)

Recovery

WB

P. ovale

LM

[71]

Libourne

1990

M

Comores

< 6 months

F

39 years

1 month (on the day)

Recovery

WB

P. falciparum

LM

[72]

Le Chesnay

2002

F

19 years

Africa

4 years

M

81 years

13 days (4 days)

Death

RBCs

P. falciparum

LM, IFAT, PCR (IFAT, PCR)

[73]

Tourcoing

2013

N/A

Endemic area

3 years

F

75 years

14 days (8 days)

Death

RBCs

P. falciparum

LM (IFAT, PCR)

[74]

Switzerland

Zurich

1999

M

30 years

Cameroon

6 years

M

70 years

14 days (22 days)

Death

RBCs, FFP

P. falciparum

LM (IFAT, PCR)

[75]

Austria

Wien

1929

M

Endemic area

10 years

N/A

14 days

Recovery

WB

P. vivax

LM

[76]

Italy

Liguria

1963

N/A

N/A

M

Premature

28–40 days

Recovery

WB

P. malariae

LM

[77]

Liguria

1963

N/A

N/A

F

8 years

1–13 days

Recovery

WB

P. vivax

LM

[78]

Liguria

1964

N/A

N/A

F

6 years

Multiple transfusions (4 months)

Recovery

WB

P. vivax

LM

[78]

Sicily

2005

M

Philippine

F

35 years

Multiple transfusions (4 months)

Recovery

WB

P. malariae

LM

[79]

Veneto

2008

N/A

N/A

F

29 years

Morocco

Multiple transfusions (2 weeks)

Recovery

RBCs

P. vivax

LM

[80]

Algeria

Algiers

1918

M

Greece

1 month

F

15 days (few days)

Recovery

WB

P. praecox b

LM (LM)

[13]

Lebanon

Beirut

2007

N/A

N/A

M

28 years

1 ½ months (2 weeks)

Recovery

RBCs

P. falciparum

LM

[81]

Beirut

2010

N/A

N/A

F

46 years

1 month (2 days)

Recovery

RBCs

P. ovale

LM

[82]

India

Shimla

2006

N/A

N/A

F

47 years

12 days (on the day)

Recovery

WB

P. falciparum

LM

[83]

Korea

 Taegu, South Corea

2000

M

21 years

Endemic area

M

1 year

15 days (5 days)

Recovery

RBCs, FFP

P. vivax

LM (LM, PCR)

[84]

Thailand

Bangkok

2011

M

teenager

Endemic area

3 weeks

F

62 years

15 days (on the day)

Recovery

RBCs

P. knowlesi

LM, PCR

[85]

Malaysia

Kuala Lumpur

2012

M

26 years

Myanmar

9 months

M

12 years

1 week (on the day)

N/A

WB

P. vivax

LM, PCR (PCR)

[86]

Sabah

2015

M

51 years

Endemic area

F

23 years

16 days (on the day)

Recovery

WB

P. knowlesi

LM, PCR (LM, PCR)

[87]

N/A data not available, WB whole blood, RBCs red blood cells, PLTs platelets, FFP fresh frozen plasma, LM light microscopy, ELISA enzyme-linked immunosorbent assay, IFAT indirect immunofluorescent antibody test, PCR polymerase chain reaction

aOnly non-endemic areas of the country if malaria endemic were included

bPossible misidentification of P. falciparum

The first report of TTM went back to 1911 and the most recent occurred in 2015, both in USA. The age of TTM case reports ranged from premature children to an 85 years old individual. The partitioning of cases in children and adults (≥ 18 years) when age was available resulted in 2 children and 39 adults for P. falciparum, 14 children and 12 adults for P. malariae, 8 children and 6 adults for P. vivax, 1 child and 3 adults for P. ovale, and 2 adults for P. knowlesi. Female versus male ratio was 1:1 for recipients and 1:6 for donors.
  1. i.

    Plasmodium species. The most common Plasmodium species detected in TTM resulted to be P. falciparum (45%) and P. malariae (30%); P. vivax, P. ovale were less frequently observed: 16 and 4% respectively; two TTM were caused by P. knowlesi (2%), and one by a mixed infection P. falciparum/P. malariae. Plasmodium praecox, an avian Plasmodium species, was described in a case report whose infection was acquired in Greece [13].

     
  2. ii.

    Species involved in fatal outcomes. The majority of fatal outcomes (11/45) was indeed caused by P. falciparum whilst all the other fatalities occurred in individuals infected by P. malariae (2/30) and P. ovale (1/4).

     
  3. iii.
    Incubation period (IP). Table 2 shows the differences in the mean incubation times for each Plasmodium species between TTM and MTM. For all species, the mean incubation time in TTM was longer, but the most relevant difference was observed for P. malariae (63.9 vs 34.6 days, p = 0.006).
    Table 2

    Mean values of transfusion-transmitted malaria (TTM) versus mosquito-transmitted malaria (MTM) incubation time in days

    Species

    TTM (95% CI)

    MTM (95% CI)a

    p valueb

    P. falciparum

    25.7 (7.4–43.9)

    13.1 (7–27)

    0.172

    P. malariae

    63.9 (43.5–84.4)

    34.8 (27–37)

    0.006

    P. ovale

    19.0 (11.7–26.3)

    13.6 (8–31)

    0.118

    P. vivax

    29.3 (12.3–46.2)

    13.4 (11–16)

    0.060

    P. knowlesi c

    15.5 (9.1–21.9)

    10.0 (/)

    0.058

    CI confidence interval

    Significance threshold p value <0.05 (in italic)

    aAs reported by Dover and Schultz [9]

    bObtained through one sample two-tailed Student’s t test, using the MTM mean value for the null hypothesis

    cA range of the mean incubation time for this species in humans was not available in literature, so a direct comparison of CIs was not possible

     
  4. iv.

    Blood component causing TTM. The vast majority of TTM cases were caused by whole blood and/or RBCs transfusion; however, two TTM cases due to platelets and one TTM case due to plasma only were reported.

     
  5. v.

    Diagnostic method used for screening (if any) and diagnosis. They are also reported in detail in Table 1. Classical Light microscopy (LM) was the diagnostic method used in virtually all cases of TTM. Only in very few cases this was complemented by serology (IFAT: first time in 1974 for a case of P. malariae occurred in US, ex-Cyprus) and/or PCR (first time in 1995 for a case of P. falciparum occurred in Canada, ex-Mali). Donor “screening” was in fact in the earlier cases the diagnosis subsequently made on the donor, classically with microscopy. Serology (IFAT) was first reported on donors in 1968 (a case of P. falciparum occurred in UK, ex-Africa, and a case of the same species occurred in US, ex-Vietnam). When reported, serology (most often IFAT) appears to be by and large the most frequent method used for donor screening.

     

Discussion

Transfusion-transmitted malaria is an alternative accidental Plasmodium infection which may cause morbidity and mortality especially in non-endemic areas where individuals have no premunition to malaria. Given the long-time span, over a century, of the case reports some countries which were endemic several decades ago are now malaria free such as the case of Greece and Italy. Therefore, it was not possible to infer any particular geographical pattern of TTM, whose occurrence may reflect people movements due to historical events as well as the proximity to a malaria endemic areas; an example is provided by the numerous army returnees from Vietnam to USA in the late 1960s who were not identified at the time as potential malaria infected blood donors, and caused an increase of TTM cases in the following years in USA [9]. Also, a limitation of this systematic review was due to the selection of exclusively case reports in order to describe the main characteristics of each episode; thus, prevalence studies were discarded as well as data on the occurrence of “transfusion outbreaks” such as the 54 cases of P. vivax TTM reported by the WHO to have taken place in Spain in 1971 due to a single blood bank in Barcelona [14]. Further limitations are due to the intrinsic nature of a systematic review based on different reports hampering the possibility to ascertain retrospectively how reliable were the clinical history and the timing of the diagnosis for each TTM case. The majority of fatal outcomes (11/45) was indeed caused by P. falciparum whilst all the other fatalities occurred in individuals infected by P. malariae (2/30) and P. ovale (1/4). However, these other fatalities were not attributable to malaria: two deaths were due to pneumonia and one was due to the complications of a premature newborn. Furthermore, all fatalities caused by P. falciparum were observed in adults and elderly people, which may reflect other co-morbidities or a more severe prognosis of malaria in adults compared to children within non-immune populations [15].

There are important differences between malaria natural infection and TTM with respect to the incubation time and delayed diagnosis: a longer incubation period was observed for all Plasmodium species as reported by Dover and Schultz [9] despite the absence of the pre-erythrocytic phase as the infected blood component directly transmits the erythrocytic stage of the parasite, namely the merozoite, to the recipient. This paradoxical phenomenon might be explained by the small inoculum of parasites from an asymptomatic donor which requires a longer period of time to develop the clinical symptoms [6]. The incubation period of TTM case reports was confirmed to be longer than the one described in natural infections as shown in Table 2: the difference reached statistical significance (p = 0.006) in P. malariae, which is arguably the species with the longest incubation time and lowest parasite density. No other statistically significant difference was observed possibly due to the limited number of case reports, thus any interpretation must be taken with caution. Moreover, particularly in some cases of P. falciparum, the IP was surprisingly and unusually long, and, although it might explained in theory by an exceedingly small number of parasites inoculated, a reporting error cannot be excluded. Nevertheless, such potential error is expected to have occurred across all TTM cases, thus making the observation still useful to reinforce the need to extend the window of time for a malaria diagnosis in blood transfusion recipients beyond the expected IP. Moreover, according to the reported data none of the TTM cases occurred in individuals with previous history of malaria, thus ruling out the possibility of recrudescence, circulating anti-malarial antibodies (as it would be the case in malaria endemic areas), or prophylaxis which might have delayed the onset of symptoms and diagnosis. Interestingly, the incubation time of the only mixed P. falciparum and P. malariae infection was of 15 days, a nearly typical incubation time for the dominant P. falciparum species compared to the milder P. malariae which employs 35 days on average to clinically develop.

Furthermore, the observation that almost half of the TTM cases reported in this systematic review are due to P. malariae (N = 30) and P. vivax (N = 16) reinforces the need to consider these other Plasmodium species as a not negligible cause of transfusion-transmitted malaria aside from P. falciparum.

Several layers of complexity underline the risk of TTM in non-endemic areas: on one hand, the limited proportion of potentially infective donors imposes a cost-effective strategy of blood donors screening, on the other hand the accuracy of such screening needs to be optimal for the serious outcomes of TTM in malaria naïve recipients.

In most non-endemic countries the first step in the blood supply chain is an epidemiological questionnaire to assess the potential donor’s risk to be infective which may result in a deferral for two groups of individuals: (i) those who were born and had lived for several years in malaria-endemic areas and (ii) those who were born and are resident in non-endemic areas but had visited an endemic area. According to the European guidelines individuals are acceptable as blood donors when an immunologic or molecular test for malaria is negative after at least 6 months since their last visit to an endemic area. When these donors have resided for more than 3 months in the endemic area, the deferral time may be longer. However long the deferral does not totally exclude infectious semi-immune individuals: in fact cases of TTM have been linked to donations given more than 5 years after the last potential exposure of the donor to P. falciparum and several decades in the case of P. malariae [3].

Conclusions

  1. i.

    The Plasmodium species most commonly involved in TTM were, expectedly, P. falciparum and P. malariae, but cases of P. vivax were not infrequent, either. This parasite is not known to remain so long in blood as the two other species, while it shares with P. ovale the phenomenon of hepatic hypnozoites (that, however, are not a possible source of transmission before they reach again the bloodstream).

     
  2. ii.

    Species involved in fatal outcomes. All fatal outcomes attributable to malaria were caused by P. falciparum and none by P. vivax, a parasite that has long been considered benign, although its potential to cause severe malaria has been repeatedly demonstrated in recent years [16].

     
  3. iii.

    The incubation period was longer than the average IP for mosquito-transmitted malaria, which may be a further reason for lack of suspicion and diagnostic delay.

     
  4. iv.

    Almost all TTM cases were caused by whole blood and/or RBCs transfusion, as expected, but for two cases by platelets and one by plasma only.

     
  5. v.

    Classical Light microscopy (LM) was used in all cases of TTM for diagnostic purposes. Only in very few cases this was complemented by serology and/or PCR in the more recent period. Serology (IFAT) was the most frequently used method for donor screening.

     

WHO regulations on blood donation needs to be reinforced as many of the TTM case reports observed even in the time span since blood safety guidelines were implemented could have been prevented if those guidelines had been applied with stringency. Thus, different strategies need to be combined in order to ensure the safety of blood transfusions i.e. blood donor screening by appropriate diagnostic tools, which should probably include molecular tests, and possibly parasite inactivation of the blood supply.

Notes

Abbreviations

CI: 

confidence interval

ELISA: 

enzyme-linked immunosorbent assay

EMBASE: 

Excerpta Medica dataBASE

FFP: 

fresh frozen plasma

IFAT: 

indirect immunofluorescent antibody test

LILACS: 

Latin America and the Caribbean Health Sciences Literature

LM: 

light microscopy

MeSH: 

medical subject heading

MMWR: 

morbidity and mortality weekly report

MTM: 

mosquito transmitted malaria

PCR: 

polymerase chain reaction

PLT: 

platelet

RBC: 

red blood cell

TTM: 

transfusion transmitted malaria

USA: 

United States of America

WB: 

whole blood

WHO: 

World Health Organization

Declarations

Authors’ contributions

FV and AA conceived the systematic review. FV and ZB wrote the manuscript after comments and discussion with AA, EM, GG, FP. GG performed the statistical analysis. EM was the second reviewer who double-checked the articles’ selection and data extraction. All authors read and approved the final manuscript.

Acknowledgements

We wish to thank Dr. Virginio Pietra and three anonymous reviewers for critical comments on the manuscript.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Funding

This research received no specific funding from any agency, commercial or not-for-profit sectors.

Publisher’s Note

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Centre for Tropical Diseases, Sacro Cuore-Don Calabria Hospital, 37024 Negrar, Verona, Italy
(2)
Department of Veterinary Sciences, University of Turin, Grugliasco, 10095 Turin, Italy

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