In the period studied, 557 patients attended SOUH´s emergency department with suspected malaria, 283 (50.8%) men, and 274 (49.2%) women, of which 132 (23.7%) were malaria positive, 61 (46.2%) male and 71 (53.8%) female. The presentation of cases does not have an accumulation for years but does preferably occur in the summer months, especially in August (Fig. 1). Depending on the diagnostic method used, 99 (75%), 104 (78.8%) and 131 (99.2%) positive cases were characterized by microscopy, ICT and NM-PCR respectively.
Plasmodium falciparum was the predominant species characterised, being the causal agent of 125 (94.7%) cases, followed by P. ovale with 5 cases (3.8%) and P. malariae with 2 cases (1.5%). No cases of malaria due to P. vivax or P. knowlesi were detected.
Twenty-five out of 132 cases (18.9%) were detected only by NM-PCR, so they were considered SMM. One case was detected only by microscopy neither by NM-PCR nor by ICT. The 99 positive cases detected by microscopy were considered microscopic malaria (MM), parasitemia was determined in 93 of them; 89 P. falciparum, 3 P. ovale and 1 P. malariae. Plasmodium falciparum showed a mean of 49 092 trophozoites/µl (range 100–430 000 trophozoites/µl), while for non-falciparum species the parasitemia mean was 16 150 trophozoites/µl (range: 2 600 − 36 000 trophozoites/µl).
By type of stay in an endemic area, VFR patients, who were living in Spain for a mean of 10 years (ranging between 1.5 months and 37 years), resulted to be the largest group, with 92 cases (69.7%), followed by MRA, with 33 patients (25%) and finally, T&B, with 7 patients (5.3%). In those patients who got malaria during a trip (VFR and T&B) the time they stayed in an endemic area ranged from 4 to 421 days, with a mean of 57 days (Table 1).
Table 1
Epidemiological, clinical and diagnostic parameters of malaria patients, divided by travel motive.
| Total | VFR | MRA | T&B | ρ |
N | 132 | 92(69.7%) | 33(25%) | 7(5.3%) | - |
Age (mean) | 36 | 35 | 25 | 48 | 0.005 |
Sex |
Male | 61(46.2%) | 43(46.7%) | 12(36.4%) | 6(85.7%) | 0.05 |
Female | 71(53.8%) | 49(53.26%) | 21(63.6%) | 1(14.29%) | 0.04 |
Infection country |
Equatorial Guinea | 62 (47.2%) | 36(39.1%) | 23(69.7%) | 3(50%) | 0.01 |
Nigeria | 48(36.6%) | 40(43.5%) | 8(24.2%) | 0(0%) | 0.04 |
Cameroon | 12(9.2%) | 10(10.8%) | 2(6.1%) | 0(0%) | 0.5 |
Angola | 2(1.5%) | 1(1.1%) | 0(0%) | 1(16.7%) | - |
Ivory Coast | 2(1.5%) | 2(2.17%) | 0(0%) | 0(0%) | - |
Mali | 2(1.5%) | 2(2.17%) | 0(0%) | 0(0%) | - |
Liberia | 1(0.76%) | 1(1.1%) | 0(0%) | 0(0%) | - |
India | 1(0.76%) | 0(0%) | 0(0%) | 1(16.7%) | - |
Zambia | 1(0.76%) | 0(0%) | 0(0%) | 1(16.7%) | - |
Unknown | 1(0.8%) | 0(0%) | 0(0%) | 1(14.3%) | - |
Plasmodium species |
P. falciparum | 125(94.7%) | 88(95.6%) | 31(93.9%) | 6(85.7%) | 0.6 |
P. ovale | 5(3.8%) | 3(3.2%) | 1(3.1%) | 1(14.3%) | 0.3 |
P. malariae | 2(1.5%) | 1(1.1%) | 1(3%) | 0(0%) | - |
P. vivax | 0(0%) | 0(0%) | 0(0%) | 0(0%) | - |
Coinfections 1 |
Total | 19(14.4%) | 8(8.7%) | 10(30.3%) | 1(14.3%) | 0.01 |
Filaria | 8(6.1%) | 3(3.2%) | 4(12.1%) | 1(14.3%) | 0.1 |
Geohelminths | 10(7.6%) | 2(2.2%) | 8(24.2%) | 0(0%) | < 0.001 |
Flukes | 4(3%) | 1(1.1%) | 3(9.1%) | 0(0%) | 0.03 |
Protozoa | 3(2.3%) | 1(1.1%) | 2(6.1) | 0(0%) | 0.1 |
Virus | 2(1.5%) | 2(2.2%) | 0(0%) | 0(0%) | - |
Poliparasitized (+ 2) | 7(5.3%) | 2(2.2%) | 5(15.2%) | 0(0%) | 0.01 |
Not coinfected | 113(85.6%) | 84(91.3%) | 23(69.7%) | 6(85.7%) | - |
Symptoms 2 |
Symptomatic | 71(91%) | 5 (98.2%) | 13(68.4%) | 4(100%) | 0.004 |
Fever | 49(69%) | 37(67.3%) | 8(42.1%) | 4(100%) | 0.04 |
Diarrhoea | 12(15.4%) | 9(16.4%) | 2(10.5%) | 1(25%) | 0.7 |
Abdominal pain | 16(22.5%) | 13(23.6%) | 2(10.5%) | 1(25%) | 0.4 |
Secondary symptoms3 | 55(77.5%) | 43(78.2%) | 9(47.4%) | 3(75%) | 0.03 |
Asymptomatic | 7(9%) | 1(1.8%) | 6(31.6%) | 0(0%) | 0.004 |
Unknown | 54(40.9%) | 37(40.2%) | 14(42.4%) | 3(42.9%) | - |
Type of malaria |
MM | 107(81.1%) | 83(90.2%) | 19(57.6%) | 5(71.4%) | < 0.001 |
< 2.500 trophozoites/µl | 12(12.9%) | 10(13.3%) | 2(15.4%) | 0(0%) | 0.8 |
2.500–150.000 trophozoites/µl | 75(80.6%) | 60(80%) | 10(76.9%) | 5(71.4%) | 0.5 |
> 150.000 trophozoites/µl | 6(6.5%) | 5(6.7%) | 1(7.7%) | 0(0%) | 0.8 |
Not determined | 6(6.1%) | 3(3.8%) | 3(18.8%) | 0(0%) | - |
SMM | 25(18.9%) | 9(9.8%) | 14(42.4%) | 2(28.6%) | < 0.001 |
Diagnosis delay |
< 30 days | 93(76.2%) | 73(81.8%) | 18(60%) | 3(75%) | 0.06 |
30 days-3 months | 18(14.8%) | 10(12.5%) | 7(24.1%) | 0(0%) | 0.1 |
> 3 months | 11(9%) | 5(5.7%) | 5(17.2%) | 1(25%) | 0.1 |
Unknown | 10(7.6%) | 4(5.6%) | 3(9.4%) | 3(42.9%) | - |
Chemoprophylaxis |
Correct | 3(2.3%) | 2(2.2%) | 0(0%) | 1(14.3%) | 0.1 |
Incorrect | 8(6.1%) | 7(7.6%) | 0(0%) | 1(14.3%) | 0.4 |
None | 121(91.7%) | 83(90.2) | 33(100%) | 5(71.4%) | 0.1 |
Analytic alterations 4 |
Anaemia (Hb < 11.6 g/dL for women, Hb < 13.2 g/dLfor men) | 47(20.3%) | 34(37%) | 13(39.4%) | 0(0%) | 0.8 |
Leucocytosis (> 4.8*10^3/µL) | 74(56.1%) | 53(57.6%) | 15(45.4%) | 6(85.7%) | 0.1 |
Thrombocytopenia (< 130*10^3/µL) | 0(0%) | 0(0%) | 0(0%) | 0(0%) | - |
GPT (> 45 U/L) | 13(9.8%) | 10(10.1%) | 1(3%) | 2(28.6%) | 0.1 |
GOT (> 34 U/L) | 20(15.2%) | 14(15.2) | 3(9.1%) | 3(42.9%) | 0.07 |
Bilirubin (< 1.2 mg/dL) | 18(13.6%) | 15(16.3%) | 2(6.1%) | 1(14.3%) | 0.3 |
VFR: Visiting Relatives and Friends, MRA: Migrants of recent arrival, T&B: Tourism and Business, MM: Microscopical Malaria, SMM: Submicroscopic Malaria, Hb: Haemoglobin, GPT: Glutamine-pyruvate transaminase, GOT: Glutamine-oxaloacetate transaminase.
On each parameter studied, patients whose data were not available were not taken into consideration for the calculi.
1 Patients with more than one different coinfection were considered more than once.
2 Patients presenting more than one different symptom were considered more than once.
3 Secondary symptoms include vomiting, headache, cough, shivering, asthenia and general discomfort.
4 Patients with more than one different analytical alteration were considered more than once.
By species, 30 cases out of 125 (24%) of P. falciparum, two out of five (40%) of P. ovale cases and one out of two (50%) of P. malariae cases were considered SMM. Fifteen out of the 30 SMM P. falciparum cases occurred in migrants of recent arrival (MRA) as the SMM case of P. malariae and one out of two P. ovale SMM cases (Table 2).
Table 2
Epidemiological, clinical and diagnostic parameters of malaria patients, divided by malaria type presented.
| TOTAL | SMM | MM | ρ |
N | 132 | 25(18.9%) | 107(81.1%) | |
Age (mean) | 36 | 30 | 34 | 0.2 |
Sex |
Male | 61(46.2%) | 11(44%) | 50(46.7%) | 0.8 |
Female | 71(53.8%) | 14(56%) | 57(53.3%) | 0.7 |
Travel motive |
VFR | 92(69.7%) | 9(36%) | 83(77.6%) | < 0.001 |
MRA | 33(25%) | 14(56%) | 19(17.7%) | < 0.001 |
TOURISTS | 7(5.3%) | 2(8%) | 5(4.7%) | 0.5 |
Infection country |
Equatorial Guinea | 62(47.2%) | 14(56%) | 48(44.9%) | 0.3 |
Nigeria | 48(36.6%) | 7(28%) | 41(38.2%) | 0.3 |
Cameroon | 12(9.2%) | 1(4%) | 11(10.3%) | 0.3 |
Angola | 2(1.5%) | 0(0%) | 2(1.9%) | - |
Ivory Coast | 2(1.5%) | 0(0%) | 2(1.9%) | - |
Mali | 2(1.5%) | 0(0%) | 2(1.9%) | - |
Liberia | 1(0.76%) | 1(4%) | 0(0%) | - |
India | 1(0.76%) | 1(4%) | 0(0%) | - |
Zambia | 1(0.76%) | 1(4%) | 0(0%) | - |
Unknown | 1(0.8%) | 0(0%) | 1(0.9%) | - |
Plasmodium species |
P. falciparum | 125(94.7%) | 22(88%) | 103(92.3%) | 0.1 |
P. ovale | 5(3.8%) | 2(8%) | 3(2.8%) | 0.3 |
P. malariae | 2(1.5%) | 1(4%) | 1(0.9%) | 0.3 |
P. vivax | 0(0%) | 0(0%) | 0(0%) | - |
Coinfections 1 |
Total | 19(14.4%) | 10(40%) | 11(10.3%) | < 0.001 |
Filaria | 8(6.1%) | 5(20%) | 3(2.8%) | 0.004 |
Geohelminths | 10(7.6%) | 7(28%) | 3(2.8%) | < 0.001 |
Flukes | 4(3%) | 2(8%) | 2(1.9%) | 0.1 |
Protozoa | 3(2.3%) | 2(8%) | 1(0.9%) | 0.1 |
Virus | 2(1.5%) | 0(0%) | 2(1.9%) | - |
Poliparasitized (+ 2) | 7(5.3%) | 4(16%) | 3(2.8%) | 0.02 |
Not coinfected | 113(85.6%) | 12(48%) | 96(92.9%) | - |
Symptoms 2 |
Symptomatic | 71(91%) | 8(66.7%) | 63(95.5%) | 0.006 |
Fever | 49(62.8%) | 7(25.3%) | 42(63.6%) | 0.7 |
Diarrhoea | 12(15.4%) | 1(8.3%) | 11(16.7%) | 0.4 |
Abdominal pain | 17(21.8%) | 4(33.3%) | 12(18.2%) | 0.2 |
Secondary symptoms 3 | 52(65.8%) | 8(72.7%) | 53(80.3%) | 0.5 |
Asymptomatic | 7(9%) | 4(33.3%) | 3(4.5%) | 0.006 |
Unknown | 54(40.9%) | 13(52%) | 41(38.3%) | - |
Diagnostic delay |
< 30 days | 93(76.2%) | 6(33.3%) | 87(83.6%) | < 0.001 |
30 days-3 months | 18(14.8%) | 7(38.8%) | 11(10.6%) | 0.005 |
> 3 months | 11(9%) | 5(27.7%) | 6(5.8%) | 0.009 |
Unknown | 10(7.6%) | 7(28%) | 3(2.8%) | - |
Chemoprophylaxis |
Correct | 3(2.3%) | 0(0%) | 3(2.8%) | - |
Incorrect | 8(6.1%) | 1(4%) | 7(6.5%) | 0.6 |
None | 121(91.7%) | 24(96%) | 97(90.6%) | 0.3 |
Analytic alterations 4 |
Anaemia (Hb < 11.6 g/dL for women, Hb < 13.2 g/dLfor men) | 47(35.6%) | 11(44%) | 36(33.6%) | 0.3 |
Leucocytosis (> 4.8*10^3/µL) | 72(54.5%) | 13(52%) | 61(57%) | 0.6 |
Thrombocytopenia (< 130*10^3/µL) | 0(0%) | 0(0%) | 0(0%) | - |
GPT (> 45 U/L) | 13(9.8%) | 2(8%) | 11(10.3%) | 0.7 |
GOT (> 34 U/L) | 20(15.2%) | 3(12%) | 17(15.9%) | 0.6 |
Bilirubin (< 1.2 mg/dL) | 18(13.6%) | 2(8%) | 17(15.9%) | 0.3 |
SMM: Submicroscopic Malaria, MM: Microscopical Malaria, VFR: Visiting Relatives and Friends, MRA: Migrants of recent arrival, T&B: Tourism and Business, Hb: Haemoglobin, GPT: Glutamine-pyruvate transaminase, GOT: Glutamine-oxaloacetate transaminase.
On each parameter studied, patients whose data were not available were not taken into consideration for the calculi.
1 Patients with more than one different coinfection were considered more than once.
2 Patients presenting more than one different symptom were considered more than once.
3 Secondary symptoms include vomiting, headache, cough, shivering, asthenia and general discomfort.
4 Patients with more than one different analytical alteration were considered more than once.
In addition to malaria, a concomitant imported disease was detected in 19 (14.4%) of the patients, 17 of them parasitic infections, mainly intestinal parasites, and two infections by imported viruses; one Dengue and other Chikungunya (Tables 1, 2). All coinfection cases were concomitant with falciparum-malaria, except one that was a malariae-malaria with two coinfections Schistosoma intercalatum plus Mansonella perstans. MRA, with 10 patients (52.6%) was the most frequently coinfected group, showing higher rates of geohelminth and fluke infections. Eight (42.1%) patients were VFR, and the last one was a Spanish T&B who traveled to Equatorial Guinea for tourism and got malaria and Loa loa infection. By malaria type, SMM patients were the most frequently coinfected, especially with filaria and geohelminths.
Access to clinical manifestations was possible only in 78 out of 132 positive patients (59.1%). The most common symptom was fever in 49 patients (62.8%) followed by abdominal pain and diarrhoea (Table 1, 2).
Ninety-three patients (76.2%) were diagnosed within 30 days after they arrived in Spain. In nine patients the diagnosis delay was higher than 6 months, ranging from 6 months to 6 years and 4 months. Four of the patients were MM, two of them being caused by P. ovale, presenting symptoms, presumably due to relapses, and the other two by P. falciparum, being one of those asymptomatic, and the other with symptoms compatible with malaria but attributed to an abdominal abscess. The other five were SMM, all P. falciparum infections, two of them asymptomatic and in the other cases, clinical data were not available.
Only 11 patients (8.4%) reported having followed any chemoprophylaxis, but only three performed it correctly. In all three cases, the patients acquired ovale-malaria despite taking Proguanil-Atovaquone (2) and Doxycycline (1). The rest of the patients followed incorrect chemoprophylaxis, either due to incomplete dosing in seven cases or, in one case, chloroquine was employed as chemoprophylaxis in a Cameroon travel. Among these patients, seven were VFR and the last was a Spanish tourist.
Accessing treatment data on patients´ history was possible only for 92 patients (69.7%), being this very variable but neither therapeutic failure nor drug resistance was observed (Fig. 2). Patients with malaria caused by P. ovale received conventional treatment followed by primaquine to eliminate the hypnozoites. Thirty-seven patients (40.2%) required hospitalisation, in eight cases (8.7%) with intravenous treatment. Only one patient required intensive care hospitalization, a Spanish T&B who visited Equatorial Guinea without taking prophylaxis, but no deaths from malaria were recorded, but none required intensive care hospitalization and no deaths from malaria were recorded.