Skip to main content
PMC home page
UKPMC Funders Author Manuscripts logoLink to UKPMC Funders Author Manuscripts
. Author manuscript; available in PMC: 2012 Dec 13.
Published in final edited form as: Trans R Soc Trop Med Hyg. 2005 Jan;99(1):71–74. doi: 10.1016/j.trstmh.2004.04.001

Travel as a risk factor for uncomplicated Plasmodium falciparum malaria in the highlands of western Kenya

GD Shanks a,*, K Biomndo b,1, HL Guyatt c, RW Snow c,d
PMCID: PMC3521062  EMSID: EMS50800  PMID: 15550264

Summary

In the 1980s, highland malaria returned to the tea estates of western Kenya after an absence of nearly a generation. In order to determine the importance of travel for the spread of malaria in this region, we prospectively collected blood films and travel, demographic and geographic information on well persons and outpatients on tea estates near the western rim of the Rift Valley. Risk factors for malaria asexual parasitaemia included: tribal/ethnic group, home province and home district malaria endemicity. Travel away from the Kericho tea estates within the previous two months showed an odds ratio (OR) for parasitaemia of 1.59 for well persons and 2.38 for outpatients. Sexual stages of malaria parasites (gametocytes) had an OR of 3.14 (well persons) and 2.22 (outpatients) for those who had travelled. Increased risk of malaria parasitaemia with travel was concentrated in children aged <5 years. An increase in population gametocytaemia is possibly due to increased chloroquine resistance and suppressed infections contracted outside of the tea estates.

Keywords: Plasmodium falciparum, Highland malaria, Travel, Kenya

1. Introduction

Most malaria encountered in western countries is among travellers returning from malaria-endemic areas. Population movement (migration and circular mobility) has also been implicated in the changing epidemiological risks of Plasmodium falciparum risk within Africa (Prothero, 1961; Van der Stuyft et al., 1993). In this paper we describe the effects of local, temporary travel upon the disease risks and local epidemiology of transmission among tea-estate workers in the western highlands of Kenya.

2. Materials and methods

The Kericho tea estates and their malaria epidemiology have been described in detail elsewhere (Malakooti et al., 1998; Shanks et al., 2000, 2002). The present study was conducted under a protocol approved by the Kenyan National Ethical Review Committee (SSC 484) and the US Army Office of the Surgeon General (WRAIR 682). A structured one-page questionnaire was administered by trained fieldworkers to asymptomatic persons on the Kerenga tea estate during 1999–2000 and to outpatients presenting to the Kerenga Health Centre with symptoms suggestive of malaria during 1998–2002. The questionnaire asked for information on demography, symptoms and travel to the nearby (50 km) Lake Victoria basin lowlands (<1000 m) in an area of highland (2000 m) malaria transmission. A thick and thin blood film was made for each person; negative slides were defined as those with no parasites seen after examination of 100 fields on the thick film. Highland and lowland family origin was defined as being from a tribal/ethnic group whose traditional home area was either above 1500 m (Kalenjin and Kisii) or below 1500 m (Luhya and Luo). Travel destinations were assigned a malaria risk criterion using a countrywide determination of malaria transmission potential. Districts were defined as low/unstable transmission risk or stable, endemic malaria transmission (Omumbo et al., 1998; Snow et al., 1999). Data recorded on the study forms were entered into a computer database and analysed using EpiInfo 2000 (CDC, Atlanta GA, USA) and SPSS, version 11 (SPSS Inc., Chicago, IL, USA) software.

3. Results

We investigated 10 789 outpatient presentations suggestive of clinical malaria and 2210 persons recruited at their homes on the Kerenga tea estate. Table 1 shows that generally the prevalence of asexual malaria parasitaemia (>95% P. falciparum) increased with symptoms (well person < outpatient), increasing home area (province or district), endemicity for malaria (epidemic < endemic), and travel away from the tea estates of Kericho. The same trends were seen for gametocytaemia. The majority of those harbouring gametocytes were children aged <5 years who had travelled recently: 52% of the total gametocyte reservoir among sick patients and 62% among healthy household members. Furthermore, sick children aged <5 years had rates of gametocytaemia that increased with the length of time since they had returned from travel: 4.3% for those who had returned within 2 weeks, 6.4% among those who had returned within 2–4 weeks and 8.6% among those who had returned within 4–8 weeks, compared to 2.3% among those who did not travel.

Table 1.

Risk factors for uncomplicated Plasmodium falciparum malaria in tea-estate workers in the western highlands of Kenya

Well persons (n = 2210)
 Outpatients (n = 10789)
Sample
sizea 		Asexual parasitaemia Gametocytaemia Sample sizea Asexual parasitaemia Gametocytaemia
Percentage
positive		 Odds ratio
(95% CI)b 		Percentage
positive		 Odds ratio
(95% CI)b 		Percentage
positive		 Odds ratio
(95% CI)b 		Percentage
positive		 Odds ratio
(95% CI)b
Gender
 Male 1134 10.3 NS 0.9 NS 5556 24.7 NS 2.6 NS
 Female 1073 11.6 1.4 5192 23.1 2.2
Family originc
 Lowland 1116 15.2 2.67 1.8 3.69 5226 28.5 1.62 3.1 1.77
 Highland 1015 6.3 (1.96–3.65) 0.5 (1.3–*) 5523 19.7 (1.48–1.77) 1.8 (1.36–2.3)
Tribe
 Luo 742 17.1 6.92 2.0 NS 3157 31.1 1.82 3.4 2.03
 Kalenjin 276 2.9 (3.23–15.47) 0.4 2703 19.8 (1.61–2.06) 1.7 (1.41–2.8)
Home province
 Nyanza 1452 11.9 4.42 1.2 NS 5801 24.5 1.58 2.6 1.84
 Rift Valley 303 3.0 (2.17–9.34) 0.3 2820 17.1 (1.4–1.77) 1.5 (1.28–2.64)
Home districtd
 Endemic 801 16.6 2.36 2.1 3.29 3799 29.3 1.8 3.2 1.83
 Epidemic 1374 7.8 (1.78–3.12) 0.7 (1.38–8.0) 6634 18.6 (1.64–1.98) 1.8 (1.41–2.38)
Travelled in last 2 months
 Travelled 753 14.1 1.59 2.1 3.14 4334 33.5 2.38 3.6 2.22
 No travel 1457 9.3 (1.2–2.1) 0.7 (1.34–7.47) 6455 17.5 (2.17–2.6) 1.6 (1.72–2.87)
Travel province
 Nyanza 515 13.4 12.4 1.7 NS 2756 34.4 1.95 3.7 NS
 Rift Valley 81 1.2 (1.8–*) 0.0 649 21.4 (1.58–2.4) 2.9
Travel districtd
 Endemic 295 18.0 1.58 3.1 NS 2278 37.4 1.48 4.3 1.63
 Epidemic 427 12.2 (1.02–2.44) 1.6 1922 28.7 (1.3–1.69) 2.7 (1.15–2.33)
Open in a new tab
*

NS: not significant, Upper limit not accurate using Cornfield statistic.

a

Sample sizes less than the total number in each study group reflect missing values.

b

Odds ratio with 95% confidence interval for relationships with P < 0.05.

c

Highland and lowland family origin defined as being from a tribal/ethnic group whose traditional home area was either above 1500m (Kalenjin and Kisii) or below 1500 m (Luhya and Luo).

d

Endemic and epidemic areas defined by climatic suitability (Omumbo et al., 1998).

The data presented in this study show that malaria parasitaemia and particularly gametocytaemia is associated with travel away from Kericho, particularly to highly endemic districts. Travel away from the tea estates within the previous 2 months showed an odds ratio (OR) for asexual parasitaemia of 1.59 and 2.38 for well persons and outpatients respectively. Sexual stages of malaria had an OR of 3.14 (well persons) and 2.22 (outpatients) for those who had travelled. This increased risk of malaria parasitaemia with travel was concentrated among young children who had returned more than 2 weeks previously.

4. Discussion

The first recorded epidemics of highland malaria on the western rim of the Rift Valley occurred when Kenyan soldiers recruited during the First World War (1914–1918) returned from Tanzania to their villages, infected with sufficient parasites to start an epidemic (Matson, 1957). Malaria epidemics occurred again during the Second World War (1939–1945) when a tented camp of transit soldiers placed near Kericho started a large and sustained epidemic within the tea estate work-force (Garnham, 1945). When chloroquine was effective as an antimalarial, epidemics appeared to be contained but then epidemics returned when this drug became ineffective (Shanks et al., 2000). Sulfadoxine–pyrimethamine (SP) replaced chloroquine in 1998 as the nationally recommended first-line therapy but, since 1998, the ability of SP to clear clinical infections has rapidly declined (East African Network for Monitoring Antimalarial Treatment, 2003; Shretta et al., 2000). Artemisinin-based combinations (WHO, 2001) may have a greater than anticipated public health role in areas such as Kericho where clinical infections acquired outside of the district may serve to promote localized epidemics through the introduction of new infectious reservoirs from initially poorly managed infections (International Artemisinin Study Group, 2004).

Acknowledgements

The authors wish to acknowledge the support of the administration and staff of Brooke Bond Kenya Ltd, particularly the medical staff at the Kerenga Clinic and Central Hospital whose outstanding medical system made this study possible. We thank Doctors Mark Arness, Dana Bradshaw, Ray Dunton and Jason Maguire as well as our study nurses, Michael Obonyo and Maurice Otieno, for their work in Kericho. Dr Simon Iain Hay is thanked for reviewing the manuscript. R.W.S. is a Senior Wellcome Trust Fellow (#058992) and H.L.G. is the recipient of Wellcome Trust Research Career Development Fellowship (#055100). The US Army Medical Research and Materiel Command, Ft. Detrick, Maryland funded this study. We acknowledge the support of the Kenya Medical Research Institute and this paper is published with the permission of its Director.

Footnotes

Conflicts of interest statement The authors have no conflicts of interest concerning the work reported in this paper.

References

  1. East African Network for Monitoring Antimalarial Treatment The efficacy of antimalarial monotherapies, sulphadoxine–pyrimethamine and amodiaquine in East Africa: implications for sub-regional policy. Trop. Med. Int. Health. 2003;8:860–867. doi: 10.1046/j.1360-2276.2003.01114.x. [DOI] [PubMed] [Google Scholar]
  2. Garnham PCC. Malaria epidemics at exceptionally high altitudes in Kenya. Br. Med. J. 1945;2:45–47. doi: 10.1136/bmj.2.4410.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. International Artemisinin Study Group Artesunate combinations for treatment of malaria: meta-analysis. Lancet. 2004;363:9–17. doi: 10.1016/s0140-6736(03)15162-8. [DOI] [PubMed] [Google Scholar]
  4. Malakooti MA, Biomndo K, Shanks GD. Re-emergence of epidemic malaria in the highlands of western Kenya. Emerg. Infect. Dis. 1998;4:671–676. doi: 10.3201/eid0404.980422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Matson AT. The history of malaria in Nandi. East Afr. Med. J. 1957;34:431–441. [PubMed] [Google Scholar]
  6. Omumbo J, Ouma J, Rapuoda B, Craig MH, le Suer D, Snow RW. Mapping malaria transmission intensity using geographical information systems (GIS): an example from Kenya. Ann. Trop. Med. Parasit. 1998;92:7–21. doi: 10.1080/00034989860120. [DOI] [PubMed] [Google Scholar]
  7. Prothero MR. Population movements and problems of malaria eradication in Africa. Bull. World Health Organ. 1961;24:405–425. [PMC free article] [PubMed] [Google Scholar]
  8. Shanks GD, Biomndo K, Hay SI, Snow RW. Changing patterns of clinical malaria since 1965 in a highland area of Kenya: possible role of drug resistance. Trans. R. Soc. Trop. Med. Hyg. 2000;94:253–255. doi: 10.1016/s0035-9203(00)90310-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Shanks GD, Hay SI, Stern DI, Biomndo K, Snow RW. Meteorological influences on Plasmodium falciparum malaria in the highland tea estates of Kericho, western Kenya. Emerg. Infect. Dis. 2002;8:1404–1408. doi: 10.3201/eid0812.020077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Shretta R, Omumbo J, Rapuoda B, Snow RW. Using evidence to change antimalarial drug policy in Kenya. Trop. Med. Int. Health. 2000;5:755–764. doi: 10.1046/j.1365-3156.2000.00643.x. [DOI] [PubMed] [Google Scholar]
  11. Snow RW, Craig MH, Deichmann U, le Sueur D. A preliminary continental risk map for malaria mortality among African children. Parasitol. Today. 1999;15:99–104. doi: 10.1016/s0169-4758(99)01395-2. [DOI] [PubMed] [Google Scholar]
  12. Van der Stuyft P, Manirankunda L, Delacollette C. L’approche de risque dans le diagnostic du paludismemaladie en regions d’altitude. Ann. Soc. Belge Med. Trop. 1993;73:81–89. [PubMed] [Google Scholar]
  13. WHO . Antimalaria Drug Combination Therapy. Report of a Technical Consultation. World Health Organization; Geneva, Switzerland: 2001. Roll Back Malaria. [Google Scholar]

RESOURCES