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    A, Location of Madhya Pradesh, India. B, Madhya Pradesh showing the location of Maihar and Mandla.

  • 1

    Brabin BJ, 1991. The risks and severity of malaria in pregnant women. Applied Field Research in Malaria. Geneva: World Health Organization, 1–34.

  • 2

    Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, Font F, Alonso PL, 2000. The impact of placental malaria on gestational age and birth weight. J Infect Dis 181 :1740–1745.

    • Search Google Scholar
    • Export Citation
  • 3

    Leke RFG, Djokam RR, Mou R, Leke RJ, Fogako J, Megnekou R, Metenou S, Sama G, Zhou Y, Cadigan T, Parra M, Taylor DW, 1999. Detection of Plasmodium falciparum antigen histidine rich protein 2 in blood of pregnant women: implications for diagnosing placental malaria. J Clin Microbiol 37 :2992–2996.

    • Search Google Scholar
    • Export Citation
  • 4

    Mankhambo L, Kanjala M, Rudman S, Lema VM, Rogerson SJ, 2002. Evaluation of the OptiMal rapid antigen test and species specific PCR to detect placental Plasmodium falciparum infection at delivery. J Clin Microbiol 40 :155–158.

    • Search Google Scholar
    • Export Citation
  • 5

    Singh N, Shukla MM, Sharma VP, 1999. Epidemiology of malaria in pregnancy. Bull World Health Organ 77 :567–571.

  • 6

    Sholapurkar SL, Gupta AN, Mahajan RC, 1988. Clinical course of malaria in pregnancy a prospective controlled study from India. Trans R Soc Trop Med Hyg 82 :376–379.

    • Search Google Scholar
    • Export Citation
  • 7

    Singh N, Saxena A, Srivastava R, 2003. Placental Plasmodium vivax infection and congenital malaria in central India. Ann Trop Med Parasitol 97 :875–878.

    • Search Google Scholar
    • Export Citation
  • 8

    Singer LM, Newman RD, Diarra A, Moran AC, Huber CS, Stennies G, Sirima SB, Konate A, Yameogo M, Sawadogo R, Bernwell JW, Parise ME, 2004. Evaluation of a malaria rapid diagnostic test for assessing the burden of malaria during pregnancy. Am J Trop Med Hyg 70 :481–485.

    • Search Google Scholar
    • Export Citation
  • 9

    WHO, 1996. A rapid dipstick antigen capture assasy for the diagnosis of falciparum malaria. WHO informal consultation on recent advances in diagnostic techniques for malaria. Bull World Health Organ 74 :47–54.

    • Search Google Scholar
    • Export Citation
  • 10

    WHO, 2000. New Perspectives: Malaria Diagnosis. Report of a Joint WHO/USAID Informal Consultation October 25–27, 1999. Geneva: World Health Organization. WHO/CDS/RBM/2000, 14 and WHO/MAL/2000, 1091.

  • 11

    Singh N, Mishra SS, Singh MP, Sharma VP, 2000. Seasonality of Plasmodium vivax and P. falciparum in tribal villages in central India (1987–1995). Ann Trop Med Parasitol 94 :101–112.

    • Search Google Scholar
    • Export Citation
  • 12

    Singh N, Tyagi AK, Sharma VP, 1995. Drug resistant Plasmodium falciparum in Mandla district, Madhya Pradesh. Indian J Malariol 32 :174–177.

    • Search Google Scholar
    • Export Citation
  • 13

    Singh N, Saxena A, 2005. Usefulness of rapid on-site Plasmodium falciparum diagnosis (Paracheck® Pf) in forest migrants and among the indigenous population at the site of their occupational activities in central India. Am J Trop Med Hyg 72 :26–29.

    • Search Google Scholar
    • Export Citation
  • 14

    Singh N, Saxena A, Sharma VP, 2002. Usefulness of an inexpensive, Paracheck Pf test in detecting asymptomatic infectious reservoir of Plasmodium falciparum during dry season in an inaccessible terrain in central India. J Infect 45 :165–168.

    • Search Google Scholar
    • Export Citation
  • 15

    Guthmann JP, Ruiz A, Priotto G, Kiguli J, Bonte L, Legros D, 2002. Validity, reliability and ease of use in the field of five rapid tests for the diagnosis of Plasmodium falciparum malaria in Uganda. Trans R Soc Trop Med Hyg 96 :254–257.

    • Search Google Scholar
    • Export Citation
  • 16

    Tjitra E, Suprianto S, Dyer M, Currie BJ, Anstey NM, 1999. Field evaluation of the ICT malaria Pf/Pv immunochromatographic test for detection of Plasmodium falciparum and Plasmodium vivax in patients with a presumptive clinical diagnosis of malaria in eastern Indonesia. J Clin Microbiol 37 :2412–2417.

    • Search Google Scholar
    • Export Citation
  • 17

    Mockenhaupt FP, Ulmen U, Gaertner CV, Addo GB, Bienzle U, 2002. Diagnosis of placental malaria. J Clin Microbiol 40 :306–308.

 

 

 

 

 

EVALUATION OF A RAPID DIAGNOSTIC TEST FOR ASSESSING THE BURDEN OF MALARIA AT DELIVERY IN INDIA

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  • 1 Malaria Research Centre, Field Station, Jabalpur, Madhya Pradesh, India; Civil Hospital Maihar, District Satna, Madhya Pradesh, India; District Hospital Mandla, Madhya Pradesh, India

All pregnant women who came for delivery at a district hospital in Mandla and a civil hospital in Maihar were screened for Plasmodium falciparum (placental parasitemia using a rapid test and microscopy and peripheral and umbilical cord parasitemia using microscopy alone). Two rapid diagnostic tests (RDTs), Paracheck Pf and ParaHITf, were used. At Mandla, the sensitivity and specificity of the Paracheck Pf for P. falciparum were 93% and 84%, respectively. The positive predictive values (PPVs) and negative predictive values (NPVs) were 50% and 99%, respectively. At Maihar, the sensitivity and specificity of the ParaHITf for P. falciparum were 87.5% and 97%, respectively. The PPVs and NPVs were 75.4% and 98.7%, respectively. Placental infection was significantly associated with low birth weight. The RDTs for the identification of P. falciparum were more sensitive in placental blood than the placental blood smear by microscopy. Thus, the RDTs should be useful for rapid assessment of malaria at delivery.

INTRODUCTION

Malaria in pregnancy is associated with adverse outcomes for mother and fetus, notably maternal anemia and low birth weight.1,2 In many studies, the strongest association with poor outcomes are with placental parasite density, but placental parasitemia is often not associated with peripheral parasitemia and can be diagnosed only at delivery.3,4 The problem of malaria in pregnancy had not been studied in India, although both Plasmodium vivax and P. falciparum have been detected in peripheral blood of pregnant women.5,6 Little is known about the occurrence of these parasites in placentas in the Indian subcontinent.7

Measuring the burden of malaria during pregnancy usually involves determining the presence of placental malaria infection through microscopic examination of placental blood films. However, placental blood films are often difficult to read because of the presence of cellular debris and a large number of white blood cells.8 In addition, microscopic examination of placental blood smears depends on good laboratory facilities and skilled technicians. The World Health Organization9 has repeatedly emphasized an urgent need for simple and cost-effective diagnostics tests for malaria to overcome the deficiencies of both light microscopy and clinical diagnosis.

The potential alternative to microscopy is the rapid diagnostic tests (RDTs) based on the detection of the P. falciparum-specific histidine-rich protein 2.10 The RDTs do not require extensive training, good infrastructure, and or even electricity.9 Two RDTs, Paracheck Pf (Orchid Biomedical Systems, Verna, Goa, India) and ParaHIT f (Span Diagnostics, Surat, India), were evaluated for rapid screening of P. falciparum malaria at delivery to determine placental infection in comparison with microscopy of placental blood smear as a gold standard. We also looked at the association of placental P. falciparum infection and low birth weight.

MATERIALS AND METHODS

All pregnant women with or without clinical symptoms of malaria who came to deliver at district hospital in Mandla, India from October 2002 to January 2003 and at a civil hospital in Maihar (Satna district), India (Figure 1) from May to December 2004 were screened for malaria parasites. Mandla is a tribal district with a population of 1.5 million. Malaria cases are mainly due to P. vivax in the dry hot season (March–June) and P. falciparum is the dominant infection during the monsoon and post-monsoon period.11 Chloroquine resistance in P. falciparum is common.12 The district has had two regular rounds of spraying with a synthetic pyrethroid (deltamethrin, 20 mg/m2) since 2000. Furthermore, surveillance is strengthened by hiring workers who provide radical treatment (chloroquine and primaquine) to all fever cases without examination of blood smears during monsoon and post-monsoon season, except for pregnant women who were not given primaquine. Maihar has a mixed rural, urban and tribal population (202,832). The prevalence of both P. falciparum and P. vivax was very high in adjacent villages and few deaths from malaria were recorded in 2003.13 Maihar has not had a spraying campaign since 1997.

Most women in both districts who participated in the study had a low socioeconomic status. The pregnant women and their family members were informed about the objectives of the study and the women were enrolled after informed consent was obtained. The study was reviewed and approved by the Ethics Committee of Regional Medical Research Center for tribals. The obstetrics and gynecology wards of the district hospital in Mandla (40 beds) and the civil hospital in Maihar (15 beds) have an antenatal clinic twice a week and an average of 200–300 women attend every month. However, technical expertise in diagnosing malaria at both hospitals is limited. For the study, a malaria clinic was established in the gynecology wards of both hospitals by the Malaria Research Center Field Station (Indian Council of Medical Research, Jabalpur). A clinical and obstetric history was obtained for each woman by a medical officer. Other clinical parameters (weight, temperature, pulse rate, blood pressure, fundal height, fetal heart rate, and the presence of edema or anemia) were obtained by a complete physical examination. Those with fever or a history of fever at some time during pregnancy were asked about periodicity of fever and if any drugs were used. Chemoprophylaxis was not given.

A finger prick sample of peripheral blood was collected from pregnant women during labor for thick and thin blood smears. At each subsequent delivery, which was assisted by midwives and nursing staff, the placenta was placed in a metal dish and a blood sample was collected immediately from a small incision made on the maternal side of placenta. Excess blood was removed. Another blood sample was collected from a cut made approximately half way along the umbilical cord. The placental and cord blood samples were collected by technical staff from the Malaria Research Center Field Station and used for blood smears prepared within 15 minutes of delivery and RDTs. The RDTs were evaluated only for determining placental parasitemia. The birth weight of each baby was recorded. The maximum time difference between peripheral and placental blood sampling was approximately six hours. The blood films were stained with Giemsa and examined by an experienced technician in the field laboratory using an oil-immersion lens (100× magnification). To ensure that low-grade infections were not missed, each smear examined for 15 minutes.

All placental blood samples were tested using Paracheck Pf and ParaHITf tests to detect P. falciparum. These two tests were introduced by the National Vector Borne Disease Control Program in inaccessible areas of central India where P. falciparum is a serious problem. Both the tests were conducted according to the manufacturer’s instructions as previously described14,15 in parallel with the blood smears. To minimize observational bias, the team member reading a placental RDT result was blinded to results of microscopic blood smear examination and vice versa. Each test was analyzed and the results were recorded by two independent observers in a blinded manner. The malarial parasites in each thick smear were counted against 300 leukocytes and the count was multiplied by 20 give estimates of the numbers of parasites per microliter of blood (assuming each blood sample contained 6,000 leukocytes/μL), as previously described.7 Placental malaria was defined as the presence of malaria parasites in a blood smear from the maternal side of the placenta. Low birth weight is defined as birth weight < 2.5 kg.

Diagnostic performance characteristics of the RDTs were calculated as previously described16 in comparison with microscopy of placental blood smears, which was used as the gold standard. The end points measured were the number of true positive (TP), true negative (TN), false positive (FP), and false negative (FN) samples. Sensitivity was calculated as TP/(TP + FN), specificity as TN/(TN + FP), positive predictive value (PPV) as TP/(TP + FP), and negative predictive value (NPV) as TN/(TN + FN). Test efficiency, which is the proportion of all tests that gave correct results, was defined as (TP + TN)/number of all tests, and the J index, (which is the overall measure of reliability of a diagnostic test) was defined as [(TP × TN) − (FP × FN)]/[(TP + FN)(TN + FP)]. When the data were analyzed, mixed infections of P. vivax and P. falciparum are classified as P. falciparum and a slide that contained only P. vivax was classified as a true negative because the test was not able to detect antigen of P. vivax. Furthermore, since sexual stages of malaria parasites do not cause fever, subjects who were positive by the RDT but had blood smears containing only gametocytes were considered false positives.

RESULTS

Two hundred nine pregnant women 18–45 years of age (mean ± SD = 23.86 ± 4.53 years) who came for delivery at the district hospital in Mandla were screened for malaria parasites. Parity ranged from 0 to 7. Five hundred ninety women 19–40 years of age (mean ± SD = 24 ± 5.07 years) who came to deliver at the civil hospital in Maihar were screened for malaria parasites. Parity ranged from 0 to 9.

Paracheck Pf evaluation.

District Hospital in Mandla.

Of 209 pregnant women, 25% had fever or a history of fever in the previous month. Microscopy showed malaria parasites in 30 of 209 placental smears, with P. falciparum comprising 26 (86.7%). The rest were mixed infections of P. falciparum and P. vivax (Table 1). The parasite densities ranged from 80 to 680 parasites/μL. This RDT detected malaria parasitemia in 56 (26.8%) of 209 pregnant women, including 4 mixed infections. There were 28 false-positive results and 2 false-negative results in this RDT (Table 2). The sensitivity and specificity of this RDT in detecting placental parasitemia were 93.3% and 84.4%, respectively. The PPV and NPV were 50% and 98.7%, respectively. The efficiency of this RDT was 85.6% and the J index was 0.78.

ParaHITf evaluation.

Civil Hospital in Maihar.

Of 590 pregnant women, 35% reported a history of fever. Fifty-four (9.2%) of 590 were infected with P. falciparum, 8 (1.4%) of 590 with P. vivax, and 2 (0.34%) of 590 had mixed infections of P. vivax and P. falciparum by microscopy (Table 1). The parasite density ranged from 120 to 205,830 parasites/μL, which is significantly higher than in Mandla (P < 0.0001). This RDT detected malaria parasitemia in 65 samples. Sixteen subjects had false-positive results and 7 subjects had false-negative results by this RDT (Table 3), and one had a parasite density of 2,440 parasites/μL. The sensitivity and specificity of this RDT for detecting P. falciparum parasitemia were 87.5% and 97%, respectively. The PPV and NPV were 75.4% and 98.7%, respectively. The efficiency of the RDT was 96.1% and the J index was 0.85.

Microscopic analysis of peripheral and cord blood infections.

At the district hospital in Mandla, peripheral smears were positive only in 11 (5.3%) of 209 pregnant women, of which 7 were P. falciparum and 4 were mixed infections (Table 1). The prevalence of placental malaria was 14.4% (P < 0.001). The women with negative peripheral blood smears had very low placental parasitemias (80–160 parasites/μL). Umbilical cord blood smears were also positive in 11 samples. At the civil hospital in Maihar, malaria parasites was detected in 41 (7%) of 590 peripheral smears compared with 10.8% in placental blood smears (P < 0.025). The women with negative peripheral blood smears also had low placental parasite densities (120–440 parasites/μL). Umbilical cord blood smears were positive only in 24 (4%) samples.

Association of infection with low birth weight.

Placental infection was significantly associated with low birth weight. Delivery of low birth weight infants was significantly more common in women who had placental parasitemias both at Mandla (mean ± SD = 2.19 ± 0.76 kg) and Maihar (2.47 ± 0.44 kg) than in women without placental parasitemia at Mandla (2.37 ± 0.31 kg) and Maihar (2.60 ± 0.44 kg) (P ≤ 0.025 and P < 0.05, respectively).

DISCUSSION

We tested two RDTs for detection of P. falciparum as an epidemiologic tool to assess the impact of malaria infection at delivery. Both tests had reasonably good sensitivities and specificities compared with placental microscopy. However, at lower levels of parasitemia, the sensitivity of the RDTs decreased as previously reported.9,14 The Paracheck Pf test had a sensitivity of 100% for P. falciparum with asexual parasite densities ≥ 200 parasites/μL in Mandla. The ParaHITf test did not identify one patient with a parasitemia > 2,000 parasites/μL, but in all patients negative by this test and blood smear positive, parasitemias were ≤ 500 parasites/μL. Furthermore, the specificity of the Paracheck Pf test was lower in Mandla. These results are consistent with those from Burkina Faso, in which an RDT for detecting placental parasitemia had a sensitivity of 95% and a specificity of 72%.8 Potential reasons for low specificity are detecting infections missed by microscopy, sequestered parasites, or newly treated infections. Persistent positivity of an RDT even after clearance of parasitemia was observed in our earlier studies13,14 and in other studies.3,8 Furthermore, since this evaluation was carried out mostly in asymptomatic pregnant women, it is therefore likely that the sensitivity and the specificity of both tests would increase if the evaluation had been conducted in subjects with symptoms.

Based on the examination of samples at two sites, we found that 9% and 4% of the women in Mandla and Maihar, respectively, who had placental parasitemia by microscopy tested negative by peripheral blood smear microscopy were cases with very low placental parasitemias. In Cameroon, 20% of the women who had placental malaria were negative by peripheral blood smear.3 In Ghana, microscopy of peripheral thick blood films did not detect more than half of the P. falciparum infections diagnosed by microscopy of placental blood films.17 This may occur because the peripheral parasitemia is below the threshold of microscopy or parasites may be sequestered in placental tissue and evade the circulation.17 Furthermore, although placental parasitemias were low in many women, the parasite may still exert a negative effect on maternal fetal exchange.3

In this study, babies born to mothers with placental malaria were significantly more likely to have low birth weights than babies born to apparently uninfected mothers. However, most of the babies, including those born to mothers who did not have placental parasitemias, had low birth weights. Although infections may have been present in many of the apparently uninfected pregnant women, the placental parasitemias may have been cleared before delivery. Furthermore, field studies are required to see if the high prevalence of low birth weight babies in the study areas is attributable, at least in part, to placental malaria.

For both clinical and epidemiologic reasons, sensitive methods are needed to assess placental malaria. The RDTs are viable options at the present time because they can be conducted quickly and do not require laboratory facilities or skilled personnel. Furthermore, RDTs are recommended not as a replacement for blood films but as a complementary adjunct to the tools available for the diagnosis of P. falciparum malaria and in particular as a rapid screening test for malaria during pregnancy. However, the RDTs are limited by their low sensitivities and because most do not differentiate Plasmodium species. A second-generation ParaHIT test is now available and should detect and distinguish infections by different Plasmodium species (Jani T, Span Diagnostics, unpublished data). Furthermore, the retail price of both RDTs is less than US$0.75. To ensure that this useful tool can be made available to those in greatest need, the cost of the tests should be further reduced. Thus, innovative approaches need to be developed to ensure the availability of RDTs in resource-poor areas where large number of fever cases must be screened. Excessive power limitations during working hours are a routine feature in most areas of the study sites, including hospitals without any power backup systems. Thus, RDTs should be used as epidemiologic tools in the assessment of the impact of malaria during pregnancy,8 in assessing new drug policies, and in chemoprophylactic studies in which placental parasitemia is investigated.

Table 1

Parasite prevalence by microscopic examination in pregnant women (peripheral, placental, and umbilical cord blood smear) who came for delivery at the district hospital Mandla and civil hospital Maihar, Satna, India*

Mandla No. (%)Maihar No. (%)
* Positive = positive for malaria; P. falciparum = Plasmodium falciparum; P. vivax = Plasmodium vivax.
No. of pregnant women screened209590
Peripheral smear positive11 (5.3)41 (6.9)
    P. falciparum7 (3.4)29 (4.9)
    P. vivax0 (0.0)10 (1.7)
    P. falciparum + P. vivax4 (1.9)2 (0.3)
Placental smear positive30 (14.4)64 (10.8)
    P. falciparum26 (12.4)54 (9.2)
    P. vivax0 (0.0)8 (1.4)
    P. falciparum + P. vivax4 (1.9)2 (0.3)
Umbilical cord blood smear positive11 (5.3)24 (4.1)
    P. falciparum7 (3.4)23 (3.9)
    P. vivax0 (0.0)0 (0.0)
    P. falciparum + P. vivax4 (1.9)1 (0.2)
Table 2

Results of Paracheck Pf rapid diagnostic test of placental blood testing in pregnant women delivering at the district hospital in Mandla, India

Result or performance index*
* Comparisons were made with results of microscopic examination of placental smears. CI = confidence interval.
True positives28
False negatives2
True negatives151
False positives28
Sensitivity (%)93.3 (95% CI = 76.5–98.8)
Specificity (%)84.4 (95% CI = 78.0–89.2)
Positive predictive value (%)50.0 (95% CI = 36.5–63.5)
Negative predictive value (%)98.7 (95% CI = 94.9–99.8)
Efficiency (%)85.6 (95% CI = 80.0–90.0)
J index0.78
Table 3

Results of ParaHITf rapid diagnostic test of placental blood testing in pregnant women delivering at the civil hospital in Maihar, Satna, India

Result or performance index*
* Comparisons were made with results of microscopic examination of placental smears. CI = confidence interval.
True positives49
False negatives7
True negatives518
False positives16
Sensitivity (%)87.5 (95% CI = 75.3–94.4)
Specificity (%)97.0 (95% CI = 95.1–98.2)
Positive predictive value (%)75.4 (95% CI = 62.9–84.9)
Negative predictive value (%)98.7 (95% CI = 97.2–99.4)
Efficiency (%)96.1 (95% CI = 94.1–97.5)
J index0.85
Figure 1.
Figure 1.

A, Location of Madhya Pradesh, India. B, Madhya Pradesh showing the location of Maihar and Mandla.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 5; 10.4269/ajtmh.2005.73.855

*

Address correspondence to Neeru Singh, Malaria Research Centre, Field Station, Jabalpur 482003, Madhya Pradesh, India. E-mail: neeru.singh@gmail.com or oicmrc@yahoo.co.in

Authors’ addressees: Neeru Singh, Ajay Saxena, and M. P. Singh, Malaria Research Centre, Field Station, Jabalpur 482003, Madhya Pradesh, India, Telephone: 91-761-267-2973, Fax: 91-761-267-2900, E-mails: neerusingh@gmail.com or oicmrc@yahoo.co.in and mrigendrapal@gmail.com. S. B. Awadhia, Civil Hospital Maihar, 485771, District Satna, Madhya Pradesh, India. Rita Shrivastava, District Hospital Mandla, 481661, Madhya Pradesh, India.

Acknowledgments: We thank Professor A. P. Dash (Malaria Research Centre, Delhi, Indai) for help and guidance. We also thank Span Diagnostics (Surat, India) and Orchid Biomedical Systems (Verna, Goa, India) for the test kits.

REFERENCES

  • 1

    Brabin BJ, 1991. The risks and severity of malaria in pregnant women. Applied Field Research in Malaria. Geneva: World Health Organization, 1–34.

  • 2

    Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, Font F, Alonso PL, 2000. The impact of placental malaria on gestational age and birth weight. J Infect Dis 181 :1740–1745.

    • Search Google Scholar
    • Export Citation
  • 3

    Leke RFG, Djokam RR, Mou R, Leke RJ, Fogako J, Megnekou R, Metenou S, Sama G, Zhou Y, Cadigan T, Parra M, Taylor DW, 1999. Detection of Plasmodium falciparum antigen histidine rich protein 2 in blood of pregnant women: implications for diagnosing placental malaria. J Clin Microbiol 37 :2992–2996.

    • Search Google Scholar
    • Export Citation
  • 4

    Mankhambo L, Kanjala M, Rudman S, Lema VM, Rogerson SJ, 2002. Evaluation of the OptiMal rapid antigen test and species specific PCR to detect placental Plasmodium falciparum infection at delivery. J Clin Microbiol 40 :155–158.

    • Search Google Scholar
    • Export Citation
  • 5

    Singh N, Shukla MM, Sharma VP, 1999. Epidemiology of malaria in pregnancy. Bull World Health Organ 77 :567–571.

  • 6

    Sholapurkar SL, Gupta AN, Mahajan RC, 1988. Clinical course of malaria in pregnancy a prospective controlled study from India. Trans R Soc Trop Med Hyg 82 :376–379.

    • Search Google Scholar
    • Export Citation
  • 7

    Singh N, Saxena A, Srivastava R, 2003. Placental Plasmodium vivax infection and congenital malaria in central India. Ann Trop Med Parasitol 97 :875–878.

    • Search Google Scholar
    • Export Citation
  • 8

    Singer LM, Newman RD, Diarra A, Moran AC, Huber CS, Stennies G, Sirima SB, Konate A, Yameogo M, Sawadogo R, Bernwell JW, Parise ME, 2004. Evaluation of a malaria rapid diagnostic test for assessing the burden of malaria during pregnancy. Am J Trop Med Hyg 70 :481–485.

    • Search Google Scholar
    • Export Citation
  • 9

    WHO, 1996. A rapid dipstick antigen capture assasy for the diagnosis of falciparum malaria. WHO informal consultation on recent advances in diagnostic techniques for malaria. Bull World Health Organ 74 :47–54.

    • Search Google Scholar
    • Export Citation
  • 10

    WHO, 2000. New Perspectives: Malaria Diagnosis. Report of a Joint WHO/USAID Informal Consultation October 25–27, 1999. Geneva: World Health Organization. WHO/CDS/RBM/2000, 14 and WHO/MAL/2000, 1091.

  • 11

    Singh N, Mishra SS, Singh MP, Sharma VP, 2000. Seasonality of Plasmodium vivax and P. falciparum in tribal villages in central India (1987–1995). Ann Trop Med Parasitol 94 :101–112.

    • Search Google Scholar
    • Export Citation
  • 12

    Singh N, Tyagi AK, Sharma VP, 1995. Drug resistant Plasmodium falciparum in Mandla district, Madhya Pradesh. Indian J Malariol 32 :174–177.

    • Search Google Scholar
    • Export Citation
  • 13

    Singh N, Saxena A, 2005. Usefulness of rapid on-site Plasmodium falciparum diagnosis (Paracheck® Pf) in forest migrants and among the indigenous population at the site of their occupational activities in central India. Am J Trop Med Hyg 72 :26–29.

    • Search Google Scholar
    • Export Citation
  • 14

    Singh N, Saxena A, Sharma VP, 2002. Usefulness of an inexpensive, Paracheck Pf test in detecting asymptomatic infectious reservoir of Plasmodium falciparum during dry season in an inaccessible terrain in central India. J Infect 45 :165–168.

    • Search Google Scholar
    • Export Citation
  • 15

    Guthmann JP, Ruiz A, Priotto G, Kiguli J, Bonte L, Legros D, 2002. Validity, reliability and ease of use in the field of five rapid tests for the diagnosis of Plasmodium falciparum malaria in Uganda. Trans R Soc Trop Med Hyg 96 :254–257.

    • Search Google Scholar
    • Export Citation
  • 16

    Tjitra E, Suprianto S, Dyer M, Currie BJ, Anstey NM, 1999. Field evaluation of the ICT malaria Pf/Pv immunochromatographic test for detection of Plasmodium falciparum and Plasmodium vivax in patients with a presumptive clinical diagnosis of malaria in eastern Indonesia. J Clin Microbiol 37 :2412–2417.

    • Search Google Scholar
    • Export Citation
  • 17

    Mockenhaupt FP, Ulmen U, Gaertner CV, Addo GB, Bienzle U, 2002. Diagnosis of placental malaria. J Clin Microbiol 40 :306–308.

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