plasmodium falciparum specific antibodies in...

ASSAY OF PLASMODIUM FALCIPARUM SPECIFIC ANTIBODIES IN MATERNAL AND CORD BLOOD AT THE UNIVERSITY OF PORT HARCOURT TEACHING HOSPITAL,

PORT HARCOURT , NIGERIA.f

1* 2 3 2 4 5Harcourt AM , Nwauche CA , Okpani AOU , Okerengwo AA , Gbenga O , Harcourt SL1 Department of Haematology and Blood Transfusion,

2 Department of Haematology, Blood Transfusion and Immunology, University of Port Harcourt. 3Department of Obstetrics and Gynaecology.

4Department of Chemical Pathology

5Department of Surgery.

University of Port Harcourt Teaching Hospital Port Harcourt, Nigeria.r

Corresponding Author: Amaka HarcourtEmail: [email protected]

Tel: +2348068514588

University of Port Harcourt Teaching Hospital

ABSTRACT Results: Plasmodium falciparum was the only Introduction: Detection of antibodies specific to malaria parasite specie detected. Rates of an antigen, especially IgM is a retrospective parasitaemia in maternal, placental and cord blood confirmation of exposure to a particular infection. were 28.9%, 20.0% and 13.3% respectively.ELISA Malaria infection is confirmed by detection of seropositivity rates for P.falciparum specific IgG Plasmodium falciparum specific antibodies. and IgM antibodies in maternal sera were 73.3% The aim of the study was to assess the occurrence and 64.4% respectively while those of cord sera of transplacental transmission of malaria parasites were 64.4% and 11.1% respectively.Malaria and provide evidence that the foetus is able to elicit parasites rates detected in maternal blood by humoral immune responses to the antigen in- microscopy differ significantly from that of utero. ELISA, but not so in cord blood (P=0.7475).

Methodology: Malaria parasites rates in maternal, Conclusion: Transplacental transmission of placental and cord blood samples from 45 Plasmodium falciparum occurred in the foetuses d e l i v e r i e s w e r e i n v e s t i g a t e d and is confirmed by detection of IgM specific microscopically.Levels of IgM and IgG specific to antibody in their cord blood.P. falciparum were measured by Enzyme-linked immunosorbent assay (ELISA) and the Keywords:Assay, specific, maternal, cord, seropositivity rates were determined. Socio- antibodies, seropositivity. demographic and obstetrics data of the parturient women was collected.

INTRODUCTION The various forms of Plasmodium develop at Plasmodium falciparum is the most virulent and different phases and encode hundreds of proteins most wide spread of the five species of human which are antigenic and evoke different malaria parasite. The other species are immunologic responses. MSP-1 is the most Plasmodium vivax, Plasmodium ovale , bountiful surface protein of the invasive merozoite

5, 6Plasmodium malariae and Plasmodium knowlesi stage of the P.falciparum life cycle . Detection of 1which is less common in human beings . Plasmodium falciparum specific antibodies,

especially IgM is a retrospective confirmation of an 7-9Plasmodium falciparum is the predominant specie attack of malaria infection . IgM is the first

in the sub-Saharan African. The female mosquito immunoglobulin produced in response to invading of Anopheles gambiae has been found to be its very antigen. It does not cross the placenta because of its

2effective vector and it is transmitted to human pentameric nature and large molecular weight.

3, 4beings during a blood meal by the mosquito . IgG appears following the process of antibody

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Original Article

10 better than microscopic examination of blood films class switch . Maternal IgG is known to cross in which low density parasitaemia most times go placental barrier passively to attain nearly equal

23, 24. undetectedtitre in cord blood. This has been attributed to the

small molecular weight of IgG and the presence of The aim of the study is to assess the occurrence of neonatal fc receptor (FcnR) on the placenta which transplacental transmission of malaria parasites facilitates the passage of IgG through the

11 and provide evidence that the foetus is able to elicit syncytiotrophoblastic membrane .humoral immune responses when exposed to malaria parasite antigen. The results will help The parasite is relatively protected from attack by obstetricians and paediatricians intensify malaria the immune system because most of its human life preventive measures in antenatal and postnatal care cycle is within the liver and blood cells, making it before the neonate is exposed to mosquito bites and relatively invisible to immune surveillance. The malaria infection.adhesive proteins produced by Plasmodium

falciparum on infected red cells enable the red MATERIALS AND METHODSblood cells to adhere to the walls of the small blood Study design, study area, Ethical considerationsvessels, thereby isolating (sequestering) the A cross-sectional hospital based study was parasite from passing through the general

12 conducted among parturient women after delivery circulation and the spleen .Occurrence of at the labour ward of the University of Port sequestration of parasites in the placenta is a Harcourt Teaching Hospital, Port Harcourt, virulent factor exclusively observed in Nigeria between February and May 2016. Plasmodium falciparum infection (13). This Approval for the study was obtained from the sequestration of the parasites in the placenta may Ethical Committee of the above mentioned block the microvasculature, thereby causing

1 4 hospital. The purpose of the study was explained to s y m p t o m s o f p l a c e n t a l m a l a r i a . each woman and informed consent was given by Syncytiotrophoblastic membrane damage may each of them.result from inflammation caused by the parasites.

This may increase transplacental passage of Source of data, sampling technique and Sample infected red cells to the foetus during pregnancy, size15, 16

and may result in congenital malaria .Socio-demographic data questionnaires were used to record relevant information including maternal Malaria in pregnancy with its accompanying risk age, blood group, parity, gestational age, and birth for the pregnant woman and her foetus is a weight. Systematic random sampling technique significant public health challenge. Congenital was used to obtain the women. 45 parturient malaria may result in severe anaemia, metabolic women were recruited for the study.17-19acidosis and death in infants . Studies have

shown that early gestational encounter with the Sample collection and Preparation:Five (5mls)

blood stage malaria antigen may have very serious each of maternal and cord blood were taken and

long term effects as a result of immune tolerance dispensed into EDTA and plain bottles

which can lead to increased susceptibility to respectively. EDTA blood samples were used for 20,21

oinfection in infancy and childhood . Immune blood films. Sera were stored at -20 C until used for

responses may be activated prior to birth by late the assay. Pooled blood from a slit in the placenta

gestational exposure to malaria antigen and this was used to make thick smears. Thick blood smears 22seems to improve responses to future attacks . were stained with Giemsa stain while thin blood

Congenital exposure to malaria antigen elicits films were stained with Giemsa and Leishman immune responses leading to production of stain. Two smears were made for each sample for

25antibodies against the antigen. Assay of quality assurance .

Plasmodium falciparum-specific antibodies in paired maternal and cord sera may reveal the actual burden of congenital malaria in the population

A Publication of Centre for Malaria Research & Phytomedicine 25

Journal of Malaria Research and Phytomedicine

Investigation of Malaria Parasitaemia at density (OD) < 0.5 was selected as sensitivity for delivery negative non- immune samples. The threshold for Microscopic Examination: Stained thick blood positivity was an absorbance >3 standard deviation films of maternal blood, cord blood and the above the mean of the negative non-immune placental blood were viewed under oil immersion samples. This threshold improves the reliability of

27(at X100) for malaria parasites. A minimum of the results .hundred thick film fields were examined for a

Statistical Analysis: All tests were carried out with sample to be considered negative. A blood smear the Epi Info v7 (CDC, Atlanta, USA) software at a was considered to have malaria infection if any of 95% confidence interval and a p-value less than the asexual blood parasites were seen in more than 0.05 was considered significant. Methods of three thick film fields. Thin blood smears were analysis for comparisons of distributed variables used for species identification. The contrast are described in Results.between parasite cytoplasm and red cell cytoplasm

is more pronounced with Leishman stain than 26 RESULTSGiemsa stain .

A total of 45 parturient women were included in the study. The age range was 20-46 years with mean Assay of P.falciparum specific IgG and IgM age of 30.3+ 0.8 years. The gestational age range antibodies: Seropositivity rates of P. falciparum was 36-41 weeks. Only 4 babies were born at 36 specific IgM and IgG antibodies in paired maternal weeks. The babies were all of normal birth weight and cord sera were determined using indirect (2.8-4.7kg).14 (31.1%) of the women were ELISA technique. Human anti-merozoite surface nullipara (primigravida), 10 (22.2%) were protein-1 IgM and IgG ELISA kits manufactured secundigravida while 21 (46.7%) were classified as by Alpha Diagnostic International, USA were used multigravida or multipara. to analyse the samples. All samples were assayed

for IgM and IgG at a dilution of 1:100 in Low non-specific binding (NSB) diluents. Net optical

Table 1: Frequency of P. falciparum infection by different methods of detection

Method of detection No (%) in maternal blood No. (%) in cord blood

Microscopic examination 13 (28.9%) 6 (13.3%)

Anti-MSP-1 IgM ELISA 29 (64.4%) 5 (11.1%)

Table 1 shows the frequency of P. falciparum infection by two methods of detection. By microscopic examination, 13 women (28.9%) and 6 cord samples (13.3%)were positive. Anti- Merozoite surface protein-1 IgM ELISA detected seropositivity in 29 (64.4%) maternal blood and in 5 (11.1%) cord blood.

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Assay of Plasmodium falciparum, Harcourt et al, 2019

Fig 2 shows the frequency ( seropositivity rates) of Anti MSP-1 IgG and IgM in maternal and cord sera analysed by ELISA .The seropositivity rates of IgG in maternal and cord sera were 33(73.3%) and 29(64.4%) respectively. The seropositivity rates of IgM in maternal and cord sera were 29(64.4%) and 5(11.1%) respectively. All samples that were IgM positive were also ELISA positive for IgG antibody.

Fig 1 shows frequency of Plasmodium falciparum in maternal, cord and placental blood smears by microscopy. The parasites were seen in peripheral thick blood films of 13 of the 45 parturient women (28.9%).Cord blood parasiteamia was observed in 6 samples (13.3%). Only 9 (20%) of the 45 placental smears had malaria parasite



Fig 3 is a scatter plot of correlation of cord and maternal Anti-MSP-1 IgM concentrations showing inverse correlation (r = -0.5).

Fig 4 is a scatter plot showing significant positive correlation of cord Anti-MSP-1 IgG concentration with increase in maternal IgG concentration (r =0.3, P< 0.05).

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DISCUSSIONS AND CONCLUSIONS 72% for maternal blood and 2.6% to 54.2% for cord 33, Studies have shown that malaria parasite antigen blood obtained by various studies done in Nigeria

2, 34passes through the placenta barrier and provoke .28, 29acquired immune response in the foetus .

Different immunoglobulins have been assayed in Enzyme linked immunosorbent assay of 30, 31, 28

the sera of subjects in malaria endemic area . Plasmodium falciparum-specific IgG and IgM In this study, the levels of IgM and IgG antibodies revealed that seropositivity rate was higher in in maternal and cord blood were evaluated to maternal than in cord samples and that all samples investigate transplacental transmission of malaria that were IgM positive were also ELISA positive

35parasites and immunological evidence that for IgG antibody. Desowitzet al, in a study in foetuses can elicit humoral immune responses Papua, New Guinea reported same for maternal when stimulated by malaria parasite antigen. samples but unlike this study which detected 11.1%

IgM seropositivity in cord blood samples, IgM was Plasmodium falciparum was the only species not present in cord blood samples of Papua New detected in this study. The study showed that the Guinea newborn. The variation may be attributed rates of malaria parasitaemia obtained in maternal to differences in geographical location. and cord samples respectively by microscopy were Plasmodium falciparum is more endemic in Africa

36higher than that obtained by George et al. (32) in . The presence of IgM in cord blood has been Port Harcourt, but within the ranges of 19.7% to

Table 2: Comparison of Mean Antibody concentration in Primigravid women and women with history of previous pregnancies.

Antibody Primigravid Previous Pregnancy T-test (p-value)

IgM (KU/ml) 173.5±84.5 175.5±82.7 0.6426**

IgG (KU/ml) 130.6±74.1 410.1±44.2 0.0151*

*Difference between the groups is statistically significant (p < 0.05)**Difference between the groups is not statistically significant (p >0.05)Table 2 shows comparison of mean antibody concentration in primigravid women and women with history of previous pregnancy. The difference in IgG concentration is statistically significant but not in IgM.

Table 3: Comparison of Mean maternal antibody concentration in placental parasiteamia

Placental

parasiteamia

Antibody concentration (KU/ml)

IgG IgM

Positive 42.6±14.9 18.1±3.1

Negative 32.7±7.1 16.5±1.5

T-test (p-value) 0.5448** 0.0422*

All values are expressed in Mean ± SEM (standard error of mean)*Difference between the groups is statistically significant (p0.05)Table 3 shows comparison of antibody concentrations in placental parasiteamia.The difference between antibody concentrations in placental malaria positive and negative subjects is statistically significant (T-test =0.0422, P

reported. In Gabon, anti- Plasmodium been observed to increase with age and frequency 42falciparumIgM was present in 11.9% of cord of malaria attacks . This may also be the reason for

serum samples examined (31). Xi et al.(9) reported the significant difference in IgG concentrations in Yaounde, Cameroon, P. faliciparum specific between primigravid and multigravid women IgM in 14% of cord blood samples. The results (women with previous pregnancies). Low 1gG obtained by the two methods used to investigate concentration seems to make the primigravida

43malaria parasite rate in this study confirms the more susceptible to malaria infection . IgM 32

finding by George et al, that congenital malaria in concentrations did not differ between primiparous not uncommon in Port Harcourt, Nigeria. and multiparous women because production of

IgM is soon followed by production of IgG and The seropositivity rates of Plasmodium other classes of immunoglobulin in a phenomenon

27falciparum-specific IgG and its concentrations known as antibody class switch . Moreover, were similar in paired maternal and cord sera women with previous pregnancies were more in the (P>0.05). The positive relationship between study than primigravid women.maternal and cord IgG concentrations was not surprising because 1gG crosses the placenta (37). IgM concentrations were approximately half the On the contrary, the parasite specific IgM concentrations of 1gG. This result differs slightly

35seropositivity rate and concentration in cord blood from that reported by Desowitzet al, in showing were lower than maternal level, giving an inverse that there was significant difference in IgM correlation (r=-0.05). This suggests that the concentrations between placental parasitaemia-foetuses produced IgM in utero in response to positive and negative subjects. Again, the variation

38, 39antigenic challenge . The mechanism of entry of in the two studies may be attributed to differences these antigens into foetal circulation was not in acquired immune factors between populations investigated in this study, but the predilection of (44).P.falciparum for placenta and the accompanying histopathological changes suggested by previous The result indicted high rate of IgM seropositivity studies may have allowed the passage of malaria in the mothers which may have resulted from the

28, 15, 14antigen from maternal to foetal circulation . incessant attacks of the parasite in endemic areas. It The intimate association between placental and has been demonstrated that IgM antibodies may feotal tissue may also afford the malaria antigen commonly be present in patients exposed to

30, 31entry into foetal circulation when a pregnant frequent malaria attacks . women gets infected with malaria parasite.

The ELISA measures anti-MSP-1 activity, a The significant difference in antibody combination of antibody concentration and avidity concentrations between seropositive and for the MSP-1 antigen. The use of a high threshold seronegative subjects supports the fact that Anti- of positivity, an absorbance of three standard MSP-1 antibody production occurs when the deviations above the mean of non-immune samples

27immune system is challenged with MSP-1 antigen improves the reliability of the results . ELISA 40. Antibodies specific to these blood stage variant detected IgG and IgM seropositivity in multiparae

surface antigens would indicate that an attack of but by microscopic examination, no parasite was malaria infection had occurred. Anti-MSP-1 detected. This suggests that ELISA may bemore seropositivity rate in the parturient women sensitive than light microscopy in malaria parasite indicated a high level of exposure which also studies. It is also interesting to note that the rate of reflects in the high level of malaria antibodies P. falciparum parasitaemia in cord blood detected

41found in cord blood. Pasay et al, obtained similar by the two methods clearly indicated that prenatal results. exposure to malaria antigen and in utero priming of

immune system of the foetus is not an infrequent The observed high concentration of IgG antibodies event.in multiparae may be associated with the age of the mothers because antibody concentrations have Transplacental transmission of malaria parasite

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antigens occurred in the foetuses and they were Antibodies to Plasmodium falciparum in Blood able to produce IgM antibodies– aconfirmation of Bank Donors for malaria Endemic and non-active malaria infection. With the finding of up to Endemic areas of Venezuela. American Journal 11.1% of congenital malaria in the study, it may be of Trop Med Hyg, 1999; 60(6): 948-953.necessary to investigate febrile illness in neonates 9. Xi, G, Leke, R.G.F, Thuital, L.W, Zhou, A, further with ELISA to rule out low density L e k e , R . J , M b u R , Ta y l o r D . W. parasitaemia. Further studies should characterize Congeni ta lexposure to Plasmodium the antigenic specificity of foetal P. falciparum falciparum antigen: prevalence and antigenic IgM antibody. More sero-epidemiological studies specificity of in-utero- produced anti-malarial of IgM antibodies especially as it relates to malaria immunoglobulin M antibodies. Infection and and pregnancy should be carried out and factors Immunity, 2003: 71: 1242 – 1246.associated with in utero immune priming should 10. Roitt, I.M. Essential Immunology. ELBS /

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