Downloaded 10/01/21 11:58 PM UTC JANUARY 2014 a B D U S S a L a M E T a L

Downloaded 10/01/21 11:58 PM UTC JANUARY 2014 a B D U S S a L a M E T a L

62 WEATHER, CLIMATE, AND SOCIETY VOLUME 6 Climate Influences on Meningitis Incidence in Northwest Nigeria AUWAL F. ABDUSSALAM School of Geography, Earth, and Environmental Sciences, University of Birmingham, Birmingham, United Kingdom ANDREW J. MONAGHAN National Center for Atmospheric Research,* Boulder, Colorado VANJA M. DUKIC Department of Applied Mathematics, University of Colorado, Boulder, Boulder, Colorado MARY H. HAYDEN AND THOMAS M. HOPSON National Center for Atmospheric Research,* Boulder, Colorado GREGOR C. LECKEBUSCH AND JOHN E. THORNES School of Geography, Earth, and Environmental Sciences, University of Birmingham, Birmingham, United Kingdom (Manuscript received 18 December 2012, in final form 6 August 2013) ABSTRACT Northwest Nigeria is a region with a high risk of meningitis. In this study, the influence of climate on monthly meningitis incidence was examined. Monthly counts of clinically diagnosed hospital-reported cases of meningitis were collected from three hospitals in northwest Nigeria for the 22-yr period spanning 1990– 2011. Generalized additive models and generalized linear models were fitted to aggregated monthly men- ingitis counts. Explanatory variables included monthly time series of maximum and minimum temperature, humidity, rainfall, wind speed, sunshine, and dustiness from weather stations nearest to the hospitals, and the number of cases in the previous month. The effects of other unobserved seasonally varying climatic and nonclimatic risk factors that may be related to the disease were collectively accounted for as a flexible monthly varying smooth function of time in the generalized additive models, s(t). Results reveal that the most im- portant explanatory climatic variables are the monthly means of daily maximum temperature, relative hu- midity, and sunshine with no lag; and dustiness with a 1-month lag. Accounting for s(t) in the generalized additive models explains more of the monthly variability of meningitis compared to those generalized linear models that do not account for the unobserved factors that s(t) represents. The skill score statistics of a model version with all explanatory variables lagged by 1 month suggest the potential to predict meningitis cases in northwest Nigeria up to a month in advance to aid decision makers. 1. Introduction * The National Center for Atmospheric Research is sponsored by the National Science Foundation. The strictly human pathogen Neisseria meningitidis is a gram-negative diplococcus that mainly causes menin- gitis (Rosenstein et al. 2001; Schuchat et al. 1997). De- Corresponding author address: Auwal F. Abdussalam, School of Geography, Earth, and Environmental Sciences, University of spite the existence of several bacteria that can cause Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom. meningitis, this bacterium is responsible for causing large E-mail: [email protected] epidemics [World Health Organization (WHO) 2012]. DOI: 10.1175/WCAS-D-13-00004.1 Ó 2014 American Meteorological Society Unauthenticated | Downloaded 10/01/21 11:58 PM UTC JANUARY 2014 A B D U S S A L A M E T A L . 63 The associated symptoms of meningitis may include An extensive part of Nigeria lies within the meningitis headache, fever, vomiting, and a stiff neck. The disease is belt (see appendix A). The disease primarily affects the a major public health burden in several countries around country during the dry months, beginning with the the world (Peltola 1983), but its magnitude is more pro- Harmattan (a dry and dusty northerly wind) in November found in Africa, in an area mainly in the Sahelian region and continuing through May with peak incidence during recognized as the meningitis belt by Lapeyssonnie (1963) the hottest months of March and April. During the 1996 and acknowledged by many (e.g., Greenwood 2006; epidemic, Nigeria alone reported over 100 000 cases and Harrison et al. 2009; Molesworth et al. 2002). 11 000 deaths to the World Health Organization (WHO) Although the mechanisms by which climatic factors (Mohammed et al. 2000), which is almost half of the total influence meningitis are still not well understood, it is cases reported from the 25 countries within the belt. Most believed that increased concentrations of dust, high of these cases and deaths were reported from the north- winds, elevated temperatures, and low humidity may ern part of the country, where there is a more pronounced cause damage to the nasopharyngeal mucosa (WHO dry season than in the south, and where the disease mainly 2012), thereby increasing meningitis risk. Outbreaks occurs each year. Meningitis in northern Nigeria is known have been associated with climatic and environmental in the native Hausa language as ‘‘Sankarau,’’ literally factors in the meningitis belt (e.g., Besancenot et al. meaning ‘‘the disease of stiffness,’’ obviously named be- 1997; Mueller et al. 2008; Sultan 2005; Thomson et al. cause of the stiff neck often associated with the disease, 2006; Yaka et al. 2008). The annual peak incidence of caused by inflammation of tissues that surround the brain meningitis has been found to correlate significantly with and the spinal cord. Anecdotal evidence suggests that the highest mean temperatures, and to correlate in- many people in northern Nigeria believe that the disease versely with absolute humidity and rainfall (Dukic et al. is caused by the intense heat usually experienced during 2012). Although some studies have concluded that prev- outbreaks. In Nigeria, meningitis transmission and in- alence of carriage does not vary with season (Greenwood vasion may be influenced by many factors apart from et al. 1984; Trotter and Greenwood 2007), others have climate, such as socioeconomic and cultural practices. In found a statistically significant link with seasonal and the cities, areas mostly occupied by low-income earners spatial climatic variability (Kristiansen et al. 2011). In are densely populated with many people per household, the Sahel, the hypothesis that meteorological factors and most use wood as their source of cooking fuel. Based influence the seasonality of disease transmission (e.g., on previous studies such as Hodgson et al. (2001), people Jandarov et al. 2012) and the development of invasive living in these areas are likely at higher risk and more disease is supported by the idea that the prolonged dry vulnerable to the development, carriage, and transmission season, which normally starts in the ‘‘cold dry’’ months of invasive meningitis. (November–January), may facilitate the occurrence of For the past 30 years, meningitis in Africa and Nigeria, precursory diseases that increase meningitis risk in the in particular, has been occurring in sporadic cases, out- subsequent ‘‘hot dry’’ months (e.g., Cartwright 1995). breaks, or even in large epidemics (Greenwood 2006) These previous efforts connecting climatic conditions to mainly caused by serogroup A (Greenwood and Stuart meningitis incidence suggest the possibility of predicting 2012; Riou et al. 1996). Until recently the only strategy meningitis outbreaks using environmental information. for controlling the disease has been through reactive mass Other nonclimatic factors may also play important vaccination campaigns after crossing a certain case roles in the risk of meningitis transmission. Among these threshold (WHO Working Group 1998), using poly- factors are socioeconomic, cultural, and behavioral saccharide A vaccine, and sometimes through special practices; and migration. Previous studies have estab- campaigns intended for religious pilgrims. Although the lished the association between nonclimatic factors and efficacy of this vaccine has been established, it is expen- meningitis risk—for example, previous incidences of sive and has a short period of effectiveness (Wahdan other upper respiratory tract infections (URTIs), such as et al. 1973). The introduction of the conjugate vaccine pneumococcal pneumonia (Moore et al. 1990), exposure (WHO 2012) brings hope for controlling the disease. to smoke from cooking fires (Hodgson et al. 2001), The new vaccine will not only provide longer protection overcrowding (Brundage and Zollinger 1987), disco but also prevent the disease (WHO 2012); that is, patronage (Cookson et al. 1998), and smoking (Fischer a whole population can be vaccinated proactively before et al. 1997). To attain precision in simulating and pos- meningitis epidemics are detected. Another advantage sibly predicting any kind of climate-related disease ep- of the conjugate vaccine is carriage prevention (Maiden idemic, if possible, climatic variables should be jointly et al. 2008; Vestrheim et al. 2010). Despite these advan- used with other nonclimatic factors as explanatory var- tages, since the conjugate vaccine is serogroup A specific iables (Thomson et al. 2006; Palmgren 2009). (Greenwood and Stuart 2012), other serogroups like Unauthenticated | Downloaded 10/01/21 11:58 PM UTC 64 WEATHER, CLIMATE, AND SOCIETY VOLUME 6 W135 (Decosas and Koama 2002) and C (Broome et al. a seasonal perspective, the variability of meteorological 1983) might continue to circulate, increasing the risk of conditions should relate to the variability of incidence in epidemics (Koumare et al. 1993). These other strains specific regions such as northwest Nigeria. could be introduced by travelers from outside regions b. Epidemiological data (Lingappa et al. 2003). The new conjugate A vaccine was recently adminis- Monthly counts of clinically diagnosed meningitis tered in Nigeria in 2011 (O. Kale et al. 2011, unpublished cases

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