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The following document is the final draft submitted to Weather, Climate 2

and Society. Please find the final published version below: 3

Ramírez, I.J., S. Grady, and M.H. Glantz, 2013: Reexamining El Niño 4

and cholera in Peru: a climate affairs approach. Weather, Climate and 5

Society, 5, 148–161. doi: http://dx.doi.org/10.1175/WCAS-D-12-00032.1. 6

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Reexamining El Niño and Cholera in Peru: A 9

Climate Affairs Approach 10

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Iván J. Ramírez 13

Division of Social Sciences, New College of Florida 14

(now at the Interdisciplinary Science Program, The New School, NYC) 15

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Sue C. Grady 18

Department of Geography, Michigan State University 19

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Michael H. Glantz 22

Consortium for Capacity Building, University of Colorado - Boulder 23

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28 Corresponding author address: Iván J. Ramírez, Interdisciplinary Science Program, Eugene Lang College, 29 The New School. 30 E-mail: ramirezi@newschool.edu; For more information: https://newschool.academia.edu/IvanJRamirez 31 32

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Abstract 33

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In the 1990s Peru experienced the first cholera epidemic after almost a century. The 35

source of emergence was initially attributed to a cargo ship, but later there was evidence 36

of an El Niño association. It was hypothesized that marine ecosystem changes associated 37

with El Niño led to the propagation of V. cholerae along the coast of Peru, which in turn 38

initiated the onset of the epidemic in 1991. Earlier studies supported this explanation by 39

demonstrating a relationship between elevated temperatures and increased cholera 40

incidence in Peru; however, other aspects of El Niño-Southern Oscillation (ENSO) and 41

their potential impacts on cholera were not investigated. Therefore, this study examines 42

the relationship between El Niño and cholera in Peru from a holistic view of the ENSO 43

cycle. A “Climate Affairs” approach is employed as a conceptual framework to 44

incorporate ENSO’s multidimensional nature and to generate new hypotheses about the 45

ENSO and cholera association in Peru. The findings reveal that ENSO may have been 46

linked to the cholera epidemic through multiple pathways, including rainfall extremes, La 47

Niña, and social vulnerability with impacts depending on the geography of 48

teleconnections within Peru. When the definition of an ENSO event is examined, cholera 49

appears to have emerged either during ENSO neutral or La Niña conditions. Furthermore, 50

the analysis herein suggests that the impact of El Ni~no arrived much later, possibly 51

resulting in heightened transmission in the austral summer of 1992. In conclusion, a 52

modified hypothesis with these new insights on cholera emergence and transmission in 53

Peru is presented. 54

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1. Introduction 56

It has been almost twenty years since Peru experienced the first cholera epidemic 57

after almost a century. The outbreak, associated with the El Tor strain of V. cholerae, 58

began in January 1991 along several coastal cities in Peru and then spread rapidly to 59

neighboring South and Central American countries, infecting approximately 400 000 60

people in the first year of the onset (Pan American Health Organization [PAHO] 1991; 61

Ministry of Health, Peru [MINSA] 1994). Over the next decade, an estimated 1.2 million 62

cases of cholera were documented in the region. Approximately 52.0% (703 000) of all 63

cholera cases occurred in Peru (PAHO 2008). 64

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While previous studies have shown that the diffusion of cholera in Peru was due 66

to poor water and sanitation system capacities (PAHO 1991; MINSA 1994, 44; Tauxe et 67

al. 1995; Seas and Gotuzzo 1996), the cause of the initial outbreak is still unknown. The 68

source of emergence was initially attributed to infected persons or contaminated waste 69

water dispelled from a cargo ship (Gangarosa and Tauxe 1992: 353). However, these 70

explanations were later challenged by another hypothesis which linked the cholera 71

epidemic to El Niño-Southern Oscillation (ENSO) (Epstein et al. 1993; Colwell 1996; 72

Mourino-Perez 1998). ENSO which includes El Niño (warm phase) and La Niña (cold 73

phase) is an important source of climate variability in the Latin American region, well 74

known for ecosystem and societal impacts, particularly in Peru (Lagos and Buizer 1992; 75

Glantz 2001a; Caviedes 2001). Therefore, it was proposed that marine ecosystem 76

changes associated with El Niño led to the propagation of V. cholerae along the coast of 77

Peru, which in turn initiated the onset of the epidemic in 1991 (Colwell 1996). 78

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In earlier studies, some evidence in Peru suggested that air and water temperature 79

changes contributed to cholera incidence via its ecological impacts on vibrios. For 80

example, it was shown that elevated temperatures were positively correlated with 81

diarrheal disease (Salazar-Lindo et al. 1997; Checkley et al. 2000; Lama et al. 2004) and 82

the presence of V. cholerae in water sources in Peru (Franco et al. 1997; Speelmon et al. 83

2000; Lipp et al. 2003). It was also reported that cholera incidence was strongly 84

associated with air and seawater temperatures during the 1997/98 El Niño (Speelmon et 85

al. 2000; Gil et al. 2004). More recently, researchers demonstrated how ocean-86

atmosphere interactions influenced the transport of vibrios along the coast of Peru 87

(Martinez-Urtaza et al. 2008). 88

89

Still, despite these advances in potential evidence, El Niño’s link with cholera in 90

Peru remains unclear. This is largely due to previous studies, which were limited in their 91

examination of the ENSO cycle. For example, the empirical evidence so far is mainly 92

based on temporal investigations in coastal Lima. Given the variability of ENSO’s 93

influence within Peru, the temperature-cholera association may have differed by 94

geography (e.g., coast versus jungle). Moreover, the strongest evidence is based on one 95

El Niño event in 1997/98. El Niño’s impact on the initial outbreak has yet to be examined 96

(Salazar-Lindo et al. 2008). Furthermore, the El Niño-cholera hypothesis is based upon a 97

period when there was disagreement about the timing of El Niño (World Meteorological 98

Organization [WMO] 1999; Glantz 2001, 21). Conceivably, this raises questions about 99

the definition of an ENSO event (Trenberth 1997), and the coincidence between the 100

physical impacts of ENSO and the emergence of cholera in Peru. In addition, the 101

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potential impacts of rainfall extremes and La Niña have not been explored in relation to 102

cholera, even though the former is an important teleconnection, and the latter is also 103

associated with health effects in Peru (MINSA 1999a). Finally, how social factors of 104

vulnerability, especially at the time of emergence, may have contributed to the impact of 105

ENSO on cholera is not yet known. 106

107

Therefore, the purpose of this study is to explore these gaps of knowledge in the 108

literature by examining the relationship between El Niño and cholera in Peru from a 109

holistic view of ENSO. Our goal is to better understand this association by considering 110

the many ways in which ENSO may have been linked to cholera emergence and 111

transmission in Peru. Another goal is to provide new insights on the hypothesis in order 112

to stimulate new avenues for potential research. As a conceptual framework, we employ a 113

“Climate Affairs” approach to widen the scope of analysis in relation to previous studies. 114

Climate affairs is a multidisciplinary concept used to understand climate-society 115

interactions worldwide (Glantz and Adeel 2001; Glantz 2003; Consortium for Capacity 116

Building [CCB] 2011), and in particular, societal impacts associated with ENSO (Glantz 117

2001a; 2001b). From a Climate Affairs orientation, we incorporate ENSO’s 118

multidimensional nature to generate new hypotheses about the ENSO and cholera 119

association in Peru. In addition to a literature review we also describe data about the 120

epidemic and ENSO collected during fieldwork in Peru in 2008 and 2009. These data 121

were obtained from documents, including health data and bulletins, newspaper archives, 122

and reports from Peruvian non-governmental and governmental institutions. 123

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Following this introduction is a description of the Climate Affairs approach and 125

its application in this study. The second section is a review of the El Niño-cholera 126

hypothesis in Peru. The third section recounts the current evidence in support of the 127

hypothesis and a link. Here, our focus is the literature in Peru. The fourth section 128

reexamines the relationship between El Niño and cholera in Peru using a Climate Affairs 129

approach. We begin by revisiting the temperature association and then explore: the 130

definition of an ENSO event, which includes an assessment of El Niño’s timing and 131

impacts in Peru; rainfall extremes; the La Niña factor; and social vulnerability. In the 132

final section, we summarize our findings and conclude by presenting a modified 133

hypothesis with new insights on cholera emergence and transmission in Peru. 134

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2. A Climate Affairs approach 136

Climate Affairs is a holistic approach to understanding the many facets of climate 137

(e.g., averages, extremes, variability and change) and how societies interact with climate 138

phenomena (Glantz and Adeel 2001; Glantz 2003; CCB 2011). Its basic components 139

encompass, but are not limited to: a) climate science; b) climate impacts; c) climate 140

economics; d) climate politics and policy; e) and climate ethics. Thus, it emphasizes the 141

importance of multidisciplinary efforts across physical and social sciences and 142

humanities. It also recognizes local and regional knowledge to understanding climate-143

society interactions (Glantz 2003). The concept evolved from the collaborative research 144

and program activities of Dr. Michael H. Glantz, which began in 1974 at the 145

Environmental and Societal Impacts Group (ESIG) at the National Center for 146

Atmospheric Research (NCAR). It later came to fruition as a research, training and 147

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education initiative in 2003. Currently, it continues to be implemented through the 148

Consortium for Capacity Building and its partners at the University of Colorado, Boulder. 149

150

Until now, the application of climate affairs has generally focused on capacity 151

building efforts with universities, research institutes, multilateral organizations, and 152

governments around the world. Among these activities, the transfer of knowledge on 153

ENSO, including forecasting, sectoral impacts, and societal responses, has been a central 154

theme (Glantz 1997; Glantz 2001b; Glantz 2002). In this study, Climate Affairs is 155

utilized as a research lens to highlight and integrate various aspects of ENSO that may 156

have been important for cholera emergence and transmission in Peru. Specifically, we 157

draw upon the following elements of ENSO knowledge: ENSO science, impacts, 158

economics, politics, and ethics. 159

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a. ENSO science 161

ENSO is a quasi-periodic phenomenon, composed of warm (El Niño), cold (La 162

Niña) and neutral phases, and ocean-atmosphere interactions that are basin-wide (i.e., 163

equatorial Pacific Ocean) and local (e.g., Peru). ENSO neutral refers to “average” sea 164

surface temperature (SST) conditions in the equatorial Pacific that do not qualify as warm 165

or cold phases (NOAA 2005). ENSO is monitored across the equatorial Pacific Ocean 166

basin in 4 delimited Niño regions known as: Niño 1+2, Niño 3, Niño 3.4, and Niño 4 167

(Figure 1). Interpreting the characteristics of phases can vary depending on the definition 168

of an event, the variables chosen to measure ENSO, and the Niño region of analysis 169

(Trenberth 1997; International Research Institute for Climate and Society 2008). 170

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Therefore, careful attention should be paid to how events are characterized because they 171

may affect the interpretation of quantitative associations between ENSO and health 172

outcomes (Kovats et al. 2003). 173

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b. ENSO impacts 175

ENSO’s influence on local climate (e.g., temperature and rainfall teleconnections) 176

can vary within different regions of Peru and by season. Geographically, the most notable 177

effects are storms and rains along the northern coast, an area which is typically arid; or 178

below average rains in the Southern and Central Andes (Lagos et al. 2008; National 179

Meteorology and Hydrology Services, Peru [SENAMHI] 2009). Although probable, 180

teleconnections are not deterministic because each event is unique and can vary in how it 181

develops from one period to another (Wyrtki 1975). However, it is possible to foresee 182

some potential effects on ecosystems and societies based on direct and indirect 183

observations of the environment, statistical assessments, computer modeling, and 184

historical reports of past events (Glantz 2001a, 163-173; McPhaden et al. 2006). In Peru, 185

they may include: marine ecosystem changes due to the disruption of upwelling 186

processes, terrestrial ecosystem changes (e.g., vegetation, insects and animals), impacts 187

on fisheries and agriculture, and damaged built environment due to flooding (e.g., energy, 188

water and sanitation systems) (Glantz 2001a). When ecosystem change co-occurs with 189

collapse of infrastructure, human exposure to infectious diseases can increase during 190

ENSO events (Gueri 1984; Valverde 1998; PAHO 1998a; Kovats et al. 2003). 191

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c. ENSO economics, politics, and ethics 193

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ENSO impacts on society are not only contingent on geographic location of 194

teleconnections, but also social, economic, and political factors of vulnerability that 195

contribute to climate-related disasters (Glantz 2003, 253; Cutter et al. 2009). In Peru, the 196

government and its population faced a number of challenges when cholera emerged that 197

included humanitarian emergencies (UN Office for the Coordination of Humanitarian 198

Affairs [UNDRO] 1990a ), economic restructuring, and an energy crisis (El Tiempo 199

1991; Youngers 2000); not to mention the high rates of population deprivation that 200

existed at the time (PAHO 1991). Assuming El Niño’s impacts were felt in Peru in 1991, 201

in addition to triggering the epidemic as has been suggested, climate may also have 202

exacerbated the severity of cholera transmission. It is important to highlight this context 203

in the explanation of the El Niño and cholera association because it places the cholera 204

epidemic at the intersection of ENSO and society interactions, which cross-sect 205

disciplinary boundaries (McPhaden et al. 2006). Tangentially, it also alludes to potential 206

issues of ‘climate’ justice (e.g., equity of impacts and differential vulnerabilities) that 207

may arise from these interrelationships (Glantz and Jamieson 2000; Ramírez 2012). 208

209

3. The El Niño-cholera hypothesis 210

Since the emergence of cholera in Peru, El Niño and climate have been associated 211

with cholera transmission. The link was first proposed by Epstein (1992) in a letter to the 212

editor at The Lancet. According to Epstein, once V. cholerae was introduced to the 213

coastal waters of Peru, it harbored among algae and plankton blooms and proliferated 214

because of “warming,” possibly due to El Niño or global climate change. Furthermore, it 215

was thought that human activities (e.g., eutrophication due to untreated sewage waste and 216

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agricultural activities) had also contributed to “enhanced” blooms. Thus, it was suggested 217

initially that cholera emerged as a result of climate and human-related processes (Epstein 218

1993; Epstein et al. 1993; 1994). As the mode of transmission, Epstein proposed that 219

human consumption of shellfish that feed on blooms was the initial pathway (1992; 220

1993). While El Niño seemed a likely reason for the epidemic, it was also thought that 221

further investigations were needed before causation could be deduced (Wilson et al. 222

1994,103).1 223

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In 1996 El Niño was hypothesized, with greater confidence and explanation, as 225

the most important driving factor in the epidemic (Colwell 1996). Motivating this 226

postulation were three ideas. First, the passing ship hypothesis was dismissed on the 227

grounds that a “single ship” could not explain multiple entry points along the Peruvian 228

coast. Second, there was growing evidence of positive relationships among plankton, V. 229

cholerae and cholera outbreaks in Bangladesh (Colwell 1996); furthermore, V.cholerae 230

was shown to survive freely in estuarine environments, lying dormant when 231

environmental conditions are less favorable, and increasing in concentrations when 232

conditions are optimal (Colwell and Spria 1992; Colwell 1996). Third, there were reports 233

of an ‘extraordinary’ El Niño, which lasted from 1990 to 1995 (Trenberth and Hoar 234

1995), which was believed to coincide with the cholera epidemic. Therefore, it was 235

proposed that an El Niño influenced sea surface temperature anomalies in the equatorial 236

1 At a workshop in 1994, Dr. Rita R. Colwell, while supportive of the potentiality of a

climate mechanism, expressed her concerns about assuming causation without further

quantitative studies.

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Pacific Ocean, which in turn promoted the abundance of plankton blooms (harboring 237

bacteria) that led to cholera transmission at multiple locations on the coast (Epstein 1992; 238

Colwell 1996; Seas et al. 2000). It was also suggested that nutrient-runoff (due to heavy 239

rains) may have contributed to the rise in blooms. The mechanism by which blooms 240

invaded the inland coast was intrusion of warm waters (Colwell 1996), either by rising 241

sea levels and/or storm surges with the arrival of El Niño. Furthermore, it was suggested 242

that the original source of V. cholerae was contaminated plankton from Asia, which may 243

have been transported via eastward-flowing ocean currents induced by El Niño (Colwell 244

1996; Mourino-Perez 1998). 245

246

In 2000, the hypothesis offered by Colwell (1996) was sustained in two important 247

studies. The first study (Seas et al. 2000) identified several clinical cases of cholera 248

preceding the onset of the epidemic in several coastal cities. The finding was instrumental 249

because it suggested that the introduction of cholera occurred prior to the arrival of the 250

passing ship, dismissing that explanation and embracing the El Niño hypothesis (Epstein 251

1992; Colwell 1996; Mourino-Perez 1998). Furthermore, there was laboratory 252

confirmation of V. cholerae in water sources, including sewage, rivers, lagoons, and 253

irrigation (Gomez Pando and Pineda 1991; Madico et al. 1996) preceding cholera 254

outbreaks in Lima, Peru (Franco et al. 1997; Speelmon et al. 2000). According to Franco 255

et al. (1997), elevated temperatures precipitated a rise in bacteria, which then amplified 256

once human fecal contamination began to increase. Importantly, a second study 257

demonstrated a quantitative relationship between ENSO and cholera from 1980 to 1998 258

in Bangladesh. Cholera transmission was explained by ENSO’s teleconnected influence 259

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on local air-water temperatures and subsequently, the intrusion of plankton blooms onto 260

the coastal shore (Pascual et al. 2000). 261

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4. Recounting the evidence in Peru 263

a. Air temperature 264

Following the initial outbreak in 1991, several studies found temperature-related 265

associations that supported an El Niño and cholera link in Peru. It was shown that 266

diarrheal diseases including cholera correlated with the warmest months (e.g., austral 267

summer, Dec to Mar) in the 1990s. Specifically when temperatures increased greater than 268

19.5°C there was also an increase in cholera incidence (Madico et al. 1996; Speelmon et 269

al. 2000). Furthermore, it was estimated that an increase of 1°C in mean air temperature 270

led to increased risk (~ 8.0%) of diarrhea in children and adults (Checkley et al. 2000; 271

Lama et al. 2004). 272

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El Niño-related risk was not observed until the onset of the 1997/98 El Niño, 274

which began rapidly developing in April 1997 (WMO 1999, 29-38). Subsequently, record 275

air temperatures were observed in Peru from May to December, which meant that 276

Peruvians would not experience winter (Bell and Halpert 1998). The impacts on diarrhea 277

and cholera risk were severe. In north Lima, diarrhea rose by 35.0% in children and 47.5 278

% in adults during the winter of 1997 (Salazar-Lindo 1997; Lama et al. 2004). In terms of 279

cholera, after a decline in 1996, cases began to noticeably rise in July 1997. The first 280

outbreaks were reported in southern Peru, where a cholera emergency was declared by 281

September (MINSA 1998a). 282

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283

According to MINSA, the greatest burden of diarrheal disease was observed 284

during the austral summer in 1998 (MINSA 1998d; Huanca 2004). Speelmon et al. 285

(2000) reported that 88.0% of cholera cases in Lima occurred from January to May. It 286

was also estimated that El Niño conditions contributed to an excess of 6225 daily 287

admissions of children with diarrhea (Checkely et al. 2000). Overall in 1998, the number 288

of cholera cases in Peru rose by 112.0% from the previous year (MINSA 2008). MINSA 289

attributed the rise in cholera and diarrheal disease to El Niño (1998a; 1998c; 2000). 290

291

b. Sea surface conditions 292

Other studies in Peru focused on the effects of sea surface conditions on V. 293

cholerae and cholera incidence along the coast of Peru. In one study, Lipp et al. (2003) 294

found that V. cholerae was significantly correlated with air temperature increases every 295

January to March from November 1998 to March 2000. Furthermore, V. cholerae was 296

detected in plankton samples at 3 coastal sites (Trujillo – North, Lima – Central, and 297

Arequipa – South). Interestingly, coastal seawater temperature was not a significant 298

factor. In a later study, Gil et al. (2004) revisited the same study areas as Lipp et al. 299

(2003), but included one additional site at Callao (considered part of the greater Lima). 300

They also measured environmental variables in relation to cholera incidence and 301

extended the time period to begin in October 1997. In this study, monthly cholera 302

incidence was strongly associated with elevated seawater temperature during the austral 303

summer of 1998. Like the previous study, V. cholerae was detected in the seawater; it 304

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supported the existence of a coastal environmental reservoir linked to seawater changes 305

(Gil et. al 2004). 306

307

More recently, the hypothesis has gained further support in a study that modeled 308

equatorial waves during the 1997/98 El Niño with the occurrence of a proxy vibrio strain 309

called Vibrio parahaemolyticus (Martinez-Urtaza et al. 2008). Using sea height anomaly 310

and upper ocean heat content to represent El Niño, the authors showed that the 311

distribution of index cases of cholera followed a pattern along the west coast of South 312

America, similar to the oceanic parameters. Coincidently, this pattern also resembled 313

locations where cholera was first identified in 1990/91, according to Seas et al. (2000). 314

This was the first study to demonstrate how vibrios and their reservoirs may have 315

traveled via ocean waves and upon arrival (i.e., against the continental boundary) 316

dispersed along the coastal environment of Peru (Martinez-Urtaza et al. 2008). 317

318

c. Summary 319

In sum, descriptive and statistical studies have shown a climate link, both direct 320

and indirect, with cholera, V. cholerae, and environmental reservoirs in Peru. The 321

associations were based on inland and coastal water temperatures during the austral 322

summer and climate thresholds which suggested that elevated temperatures led to a 323

greater number of diarrheal disease in the 1990s. With respect to El Niño, there was an 324

apparent association with the 1997/98 event. While these studies provided some evidence 325

for a climate-cholera connection in Peru, there are still many unanswered questions. In 326

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the following section, we explore several factors which we argue are critical to 327

understanding El Niño’s link to cholera emergence and transmission in Peru. 328

329

5. Reexamining El Niño and cholera in Peru 330

331

Here, we use a Climate Affairs approach to reexamine the association between El 332

Niño and cholera in Peru using a broader conception of ENSO. Our discussion begins by 333

revisiting the temperature-related association followed by an exploratory investigation 334

that highlights the following ENSO characteristics: the definition of an ENSO event; 335

rainfall extremes; the La Niña factor; and social vulnerability. 336

337

a. Revisiting the temperature association 338

While a temperature-related association is plausible because of its potential 339

impact on the reproduction of vibrios, its generalization in Peru is limited by its 340

geographic scope. This is due to the fact that previous findings in Peru were generally 341

based on temporal observations in Lima, which is located on the central coast. Given the 342

country’s diverse physical regions, which range from a low-lying coast to highlands and 343

jungle in the east (Figure 2), it is possible that there may have been regional variations of 344

the temperature association within Peru. For instance, in Loreto, a jungle region located 345

in northeast Peru, seasonal patterns of cholera were indeed different from the Lima time 346

series (Figure 3 [a]). In Lima, peaks in cholera cases were observed from February to 347

April from 1993 to 1998. In contrast, cholera increased in Loreto from mid-summer to 348

early autumn (Jul to Oct) in 1993, 1995, and 1998; there were also peaks in May of 1993 349

and 1998 (Figure 3 [b]). In general, the temporal pattern of cholera in Loreto was less-350

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well defined and lagged in time compared to Lima. This difference may reflect, 351

particularly in the case of 1998, the geography of El Niño-related teleconnections by 352

region. For example, on the central coast El Niño may contribute to warmer and wetter 353

than average conditions from June to August (SENAMHI 2004); in the Amazon, it may 354

contribute to rainfall deficit in November and December (Marengo 1999; Marengo et al. 355

2008). These differences highlight the importance of region, which suggest not only that 356

different temporal pathways might exist, but also that different climate pathways may 357

have impacted cholera transmission. 358

359

The temperature-related association is also limited because El Niño’s link to 360

cholera is based on one event in 1997/98. For example, even though Lama et al. (2004) 361

found a strong association between El Niño and diarrheal disease in 1998, it was also 362

shown that prior El Niños were not statistically significant.2 One reason for this outcome 363

may have been the short length of time series (i.e., 1991 to 1998), which seems to limit 364

studies in Peru because they have generally been cross-sectional and do not include the 365

initial outbreak time segment. 366

367

b. Definition of an ENSO event 368

One important assumption of the El Niño-cholera hypothesis is that El Niño 369

conditions were present in order to impact the transport and reproduction of contaminated 370

2 It is important to note that it is unclear how Lama et al. (2004) identified El Niños.

According to their study which cited data from NOAA, the onset dates were: 1)

September 1991; 2) April 1993; and 3) September 1994.

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plankton off the coast of Peru, potentially from October 1990 to January 1991(i.e., based 371

on Seas et al. [2000]). Although an El Niño was suspected during that time, there were 372

also varying reports about the timing of El Niño(s) in the early 1990s. For example, for 373

some researchers it was the longest El Niño of the century, lasting five years from 1990 374

to 1995 (Trenberth and Hoar 1996). For others, it endured from September 1991 to July 375

1993 (McPhaden 1994; Kessler and McPhaden 1995). It was also estimated that 3 events 376

took place from: (1) March 1991 to June 1992; (2) 1993 (Feb/Mar to Oct); and (3) 1994 377

(Jun to Nov) (Goddard and Graham 1997). Importantly, Peruvians questioned the view of 378

an El Niño in 1991 because they noticed they were catching near-record-setting anchovy 379

landings, highly unlikely during a warm episode (Flores 1998; Glantz 2001, 21). 380

Therefore, two fundamental questions about the hypothesis are raised. The first is 381

whether an El Niño was in development at the time of emergence. The second is whether 382

El Niño’s effects were observed in Peru. The latter question is important because it may 383

explain the transport and coastal intrusion component of the hypothesis. 384

385

To address the question about El Niño’s timing, we explored the definition of an 386

ENSO event, which determines the characteristics of an episode including its beginning 387

and end dates (Trenberth 1997). The definition is important because it may affect how 388

one characterizes the relationship between El Niño and cholera emergence, which is 389

dependent on whether the two events coincided in time. To illustrate this point, we 390

compared sea surface temperature anomalies (SSTA) in 3 Niño regions with monthly 391

cholera cases in Peru from 1990 to 1992. As a definition, we chose the operational one 392

used by NOAA, which is commonly employed to identify an event (See NOAA 2012). 393

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Figure 4 shows the SSTA and cholera time series and Table 1 lists El Niño and La Niña 394

events, respectively. According to the Niño 4 region, the first possible cases of cholera 395

(identified by Seas et al. [2000]) and the onset of the epidemic occurred in the midst of a 396

prolonged El Niño (26 months) that developed in July 1990 (event [a]). The timing in the 397

Niño 4 region, which represents the western equatorial Pacific, sustains the El Niño-398

cholera hypothesis and suggests a time delay of several months between El Niño and 399

cholera emergence. On the other hand, regions Niño 3.4 and Niño 1+2, which represent 400

the central and eastern equatorial Pacific, indicate that El Niño conditions followed the 401

initiation of the epidemic, beginning in May (event [c]) or November (event [d]) of 1991. 402

Using Pearson’s correlation analysis, we explored these associations further and found 403

the strongest link between cholera and SSTA in the Niño 1+2 region (r = 0.42, p-value = 404

0.010). This finding is important because the Niño 1+2 region includes coastal and 405

equatorial upwelling near Peru and Ecuador (Glantz 2001, 60), which exhibited non-El 406

Niño conditions preceding and during the initial outbreak in January 1991 (see Figure 4 407

and Table 1 [d]). In other words, it may have been La Niña and ENSO neutral rather than 408

El Niño that contributed to cholera emergence in Peru. 409

410

EL NIÑO’S EFFECTS IN 1991? 411

To explore the timing of El Niño further, we examined the literature to 412

identify El Niño-related impacts on ecosystems and climate in Peru. One potential effect 413

we looked for is the impact on anchovy, pelagic fish whose habitat and food supply are 414

altered when upwelling weakens during El Niños (Chavez et al. 2008). According to the 415

Peruvian Marine Institute, 1991 was described as a year with cold coastal waters and 416

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good for anchovy catch (Pizarro 1999), which implied that average SST conditions were 417

present off the coast of Peru and that upwelling and marine biological productivity was 418

normal too. We also looked for ecosystem impacts in other areas of the eastern Pacific 419

Ocean. For example, biological impacts (associated with El Niño) were reported off the 420

coast of Costa Rica (e.g., coral bleaching and mortality) in March to April 1992 (Jimenez 421

and Cortes 2001), in the Galapagos (e.g., penguin populations declined associated with 422

lower food supply) from 1991 to 1993 (Hernan Vargas et al. 2006), and off the coast of 423

Chile (e.g., changes in planktic fauna species) from November 1991 to March 1992 424

(Marchant et al. 1998). With regard to impacts on local climate (teleconnections), 425

NOAA reported intense rains on the north coast of Peru during the austral summer of 426

1992. Apparently, an El Niño which began developing in mid-1991 was in a mature 427

phase (NOAA 1992; 1993). Supporting the NOAA observations were local newspaper 428

accounts that documented storms, inundations and disasters (El Tiempo 1992a,b). As 429

mentioned previously, the north coast of Peru is strongly associated with El Niño and 430

rains (Lagos et al. 2008) and is therefore a good indicator of a warm event in Peru. 431

Although speculative, biological changes in marine ecosystems along with physical 432

impacts in mid-to-late 1991/early 1992 support the idea that El Niño may have followed 433

rather than led the onset of the cholera epidemic in 1991. 434

435

c. Rainfall extremes 436

In addition to temperature, rainfall extremes are important El Niño 437

teleconnections. In Peru they may have been a pathway for cholera transmission. Rainfall 438

extremes can influence the concentration and transport of bacteria and environmental 439

20

hosts (Ruiz-Moreno et al. 2007; Hashizume et al. 2008; Mendelsohn and Dawson 2008; 440

Reiner Jr. et al. 2011; Bertuzzo et al. 2012; Rinaldo et al. 2012). In particular, heavy rains 441

can contribute to nutrient run-off, which in turn, may positively affect plankton blooms in 442

coastal areas (Constantin de Magny et al. 2008; Jutla et al. 2010); furthermore, wind-443

driven rain can drive coastal waters with plankton inland, thereby increasing human 444

interactions with V. cholerae (Constantin de Magny et al. 2008). Heavy rains can also 445

increase cholera risk through flooding and overflow of rivers, and subsequent 446

contamination of the water supply (Kovats et al. 2003; Ruiz-Moreno et al. 2007; Reiner 447

Jr. et al. 2011). For example, during the recent cholera epidemic in Haiti, intense rains 448

increased incidence in 2010-2011 by enhancing surface run-off and transport of fecal 449

matter from open latrines to inland water sources (Rinaldo et al. 2012). In Peru, cholera 450

may have spread via rains in low-lying areas in the department of Piura (see Figure 2), 451

which reported index cases in 1991 (Ries et al. 1992). Figure 5 compares cholera cases 452

with rainfall (mm) in January to April from 1991 to 2000 in a subregion of Piura (located 453

860 km north of Lima). Cholera and rainfall increases in Piura were clearly evident in 454

1992 and 1998. Furthermore, during the onset of cholera and the first quarter of 1991 455

(i.e., Oct 1990 to Apr 1991), total rainfall in Piura was 7 mm compared to 329 mm in 456

1992 and 1842 mm in 1998. Together, these observations along with local reports suggest 457

that flooding, possibly via the breakdown of water and sanitation infrastructures, led to 458

enhanced cholera transmission in Piura (El Tiempo 1992a; 1992b; PAHO 1998b; MINSA 459

1998b; 1998d). Although elevated temperatures may have contributed to cholera 460

incidence in Lima, heavy rains may have been a more important factor in northern Peru. 461

Alternatively, rainfall deficit may have contributed to cholera transmission as well 462

21

(Codeco 2001; Pascual et al. 2002; Hashizume et al. 2008; Akanda 2009). For example, 463

in the jungle region of Loreto, which we discussed earlier, low river levels were 464

associated with cholera risk in places of poor water and sanitation infrastructures 465

(MINSA 1995; 1998b). A dry season along with elevated air temperatures can impact 466

bacteria and increase cholera risk due to limited availability of potable water (Codeco 467

2001; Huq et al. 2005). 468

469

d. The La Niña factor 470

La Niña, the cold phase of ENSO, is another pathway that may have impacted 471

cholera transmission in Peru. La Niña enhances average SST conditions (e.g., cold) in the 472

eastern equatorial Pacific Ocean. Therefore, via its positive influence on upwelling, 473

which brings nutrients to the surface waters, La Niña may have contributed to cholera 474

emergence (we discuss this pathway within a broader context of the El Niño-cholera 475

hypothesis in the final section). As well, La Niña may have increased cholera risk 476

through its own set of teleconnections (Ropelewski and Halpert 1987; Ordinola 2002; 477

NOAA 2005). During La Niña, climate in Peru is drier than average on the northern coast 478

(Ordinola 2002) and wetter than average in the Southern and Central Andes, particularly 479

in the Altiplano, which borders Bolivia and Chile (Sperling et al. 2008). Following the 480

1997/98 El Niño, rain-related disasters were reported in the highlands in February 1999. 481

Subsequently, populations were affected by floods and many were in need of assistance 482

with food, water and sanitation (MINSA 1999a). La Niña conditions along with those in 483

the tropical Atlantic were blamed (MINSA 1999b). 484

485

22

e. Social vulnerability 486

When cholera emerged in 1990/91, the Peruvian government was already 487

addressing complex emergencies, which began earlier that year in late summer/early 488

winter. The first was an earthquake in northeast Peru, which affected 70 000 and injured 489

1500 people in May 1990 (UNDRO 1990a). The second was an agricultural state of 490

emergency declared across highland regions in June 1990. It was reported that over 2 491

million subsistence farmers were gravely affected by an ongoing drought and cold 492

extremes experienced in 1989, reportedly a La Niña year; consequently, food and water 493

supplies were in decline (UNDRO 1990b). That austral winter was also the beginning of 494

“Fuji Shock,” a set of economic reforms, implemented by the then elected President 495

Alberto Fujimori (Brooke 1990). As a result of these policies, public infrastructure and 496

services were reduced including those in the health sector, where resources were already 497

limited (Cueto 2001, 107-137). Furthermore, the country was contending with an energy 498

crisis (El Tiempo 1991; Nash 1991; Youngers 2000). Power outages affecting water and 499

sanitation plants and residents were reported (El Tiempo 1991). Ultimately, these events 500

which included public policies may have aggravated the pre-existing living conditions of 501

the population, who lacked immunity to cholera, and lacked adequate water and 502

sanitation infrastructure.3 If ENSO and its influence on climate and society had an impact 503

on cholera in Peru, it could not have occurred apart from social vulnerability. 504

3 In 1991 approximately 45.0% of Peru’s population did not have access to clean water

and 59.0% were without sanitation services. In rural areas, conditions were much worse;

there, less than one-third of the population had access to clean water and other basic

services (PAHO 1991).

23

6. Summary and conclusions 505

Although cholera was eradicated in Peru in 2002, it remains a potential threat to 506

the country and region because of the recent emergence in Haiti, which was also 507

associated with ENSO (Enserink 2011). Therefore, this research is timely, and supports 508

other studies which seek to understand how climate variability affects cholera epidemics 509

(Pascual et al. 2000; Koelle et al. 2005; Constantin de Magny et al. 2007; Reiner et al. 510

2011; Reyburn et al. 2011). In sum, this study examined the relationship between El Niño 511

and cholera in Peru using a climate affairs approach. From this holistic view, we 512

explained cholera incidence from a broader conception of ENSO, one which includes not 513

only temperature, but also geographic variability, how we define ENSO, the impacts of 514

rainfall and La Niña, and underlying social dimensions. In doing so, we linked ENSO to 515

cholera in Peru through multiple pathways. 516

517

Specifically, our study showed that a temperature-cholera association may have 518

differed temporally between regions because of geography and the variability of El Niño 519

teleconnections within Peru (e.g., varying cholera peaks between coast and jungle). It was 520

also shown that another pathway may have been rainfall extremes (e.g., torrential rains on 521

the north coast), which impacted infrastructure, river levels and water supply, leading to 522

increased exposure to cholera. Heavy rains were likely a critical factor in 1992 and 1998 523

during El Niños. Importantly, when we explored the definition of an ENSO event, our 524

analysis revealed that cholera may have emerged in Peru during ENSO neutral or La 525

Niña rather than El Niño conditions. Our interpretation which disputes the presence of El 526

Niño in the prior and onset months of the cholera epidemic was supported by a 527

24

significant correlation between cholera and sea surface temperatures in the Niño 1+2 528

region, an area proximate to the Peruvian coast. Our study also highlighted that biological 529

and physical evidence of El Niño was not observed until the end of 1991, which supports 530

further that El Niño did not coincide with the initial epidemic. In light of these findings, 531

our study overall suggests that the cholera epidemic in Peru was likely already underway 532

by the time El Niño developed in 1991. Therefore, the warm phase of ENSO could not 533

have impacted the onset or initiation of the cholera outbreak in Peru. 534

535

However, our findings do not preclude an ENSO or climate contribution. Instead our 536

study suggests that non-El Niño conditions may have played a contributive role during 537

cholera emergence. Non-El Niño conditions are indicative of rich biological productivity 538

due to upwelling processes which may have positively influenced plankton reservoirs in 539

late 1990/early 1991. Concurrently, multiplication of plankton and vibrios in the coastal 540

zone may have occurred because of eutrophication due to human activities (e.g., 541

agriculture run-off and sewage dumping) (Epstein 1992; 1993). Vibrios may have also 542

increased in population due to seasonal warming of SST and air temperatures due to the 543

onset of summer in December. This association is plausible given that cholera and 544

diarrheal disease were correlated with warmer months following the initial outbreak in 545

January 1991 (Salazar-Lindo 1997; Checkley et al. 2000; Speelmon et al. 2000). Human 546

transmission may have taken place by consumption of contaminated seafood (e.g., 547

shellfish), which was an initial vehicle of infection in Peru (MINSA 1994), and suggested 548

originally by Epstein (1993). Once cholera was introduced to the coastal inland, local 549

transmission was amplified by human-fecal contamination (Franco et al. 1997), and then 550

25

propagated under the social vulnerability context which we described earlier and was 551

reported widely (PAHO 1991; MINSA 1994; Cueto 2001, 107-137). 552

553

It was more likely that El Niño’s impact arrived much later than the initial outbreak in 554

1991, contributing to cholera transmission in the austral summer of 1992 via the 555

mechanism proposed by Colwell (1996). More specifically, this multi-pathway is as 556

follows: with the arrival of Kelvin waves which carry warm waters from the western 557

Pacific, SST increased and sea level rose along the coast of Peru. The pool of anomalous 558

warm waters positively affected the reproduction of vibrios living in the coastal zone. 559

With respect to plankton reservoirs, their proliferation was potentially influenced by three 560

factors associated with nutrient enrichment. The first factor is related to human activities 561

(Epstein 1993; Epstein et al. 1993), which we mentioned previously. The second factor is 562

nutrient enrichment by run-off due to high river discharge (Jutla et al. 2011), which may 563

occur during strong El Niños (Lavado Casimiro et al. 2012). Jutla et al. (2011) report that 564

this is the main driver of plankton blooms rather than rising SST in coastal Bangladesh, 565

and therefore, this may have been an important pathway in 1992. The third factor is 566

upwelling, which may appear counterintuitive at first. However, while it is likely that 567

equatorial upwelling (near Ecuador) is negatively affected during El Niños (NOAA 568

2005), it is not always true for coastal upwelling near Peru. There, upwelling diminishes 569

by geographic extent (shifting closer to the coast), but continues to persist and even 570

intensify during warm episodes as winds blowing towards the coast increase (Enfield 571

1981). It explains why plankton species could remain high under warm anomalous SST 572

conditions during past El Niño events (Barber and Chavez 1983; Chavez 1996). Once 573

26

vibrios and reservoirs multiplied on the coast, rising sea-level heights and storm surges 574

led to coastal intrusion transporting organisms to the inland, where teleconnections (e.g., 575

warmer air and water temperatures and heavy rains) affected their reproduction and 576

distribution. Impacts on cholera, however, varied by geographic region, depending on the 577

hydrology (Akanda 2009; Bertuzzo et al. 2012; Rinaldo et al. 2012), infrastructure and 578

immunity levels of the population (Mari et al. 2011; Rinaldo et al. 2012). Within a poor 579

infrastructure context, rainfall impacts led to collapse of water and sanitation systems 580

along the coast, more likely in the north where El Niño impacts are strongest, resulting in 581

heightened transmission in the summer months of 1992. 582

583

Although we cannot explain the initial source of cholera emergence in Peru, we can 584

assume that if El Niño conditions were not present in the eastern equatorial Pacific during 585

the initial outbreak, it is unlikely that distant vibrios travelled via El Niño-related ocean 586

waves in 1990/91. The answer to the origins of cholera in Peru is more likely to be found 587

in an explanation that combines information from existing hypotheses (both human 588

importation and climate) with current advancements in the microbiology and genetics of 589

V. cholerae. Most recently, the latter has helped confirm the source of cholera emergence 590

in Haiti (Chin et al. 2011), which attributed the introduction to foreign importation by 591

asymptomatic individuals (Piarroux et al. 2011; Cravioto et al. 2011). In Peru, the idea of 592

human importation remains a viable pathway to investigate given a recent genetic study 593

that suggests the Latin American strain of V. cholerae came from Africa; possibly by 594

human migration (during some undefined time period) following the arrival of the 595

seventh-pandemic in that continent in the 1970s (Lam et al. 2010). It may help explain 596

27

how V. cholerae may have become indigenous to the coast of Peru prior to the emergence 597

in 1990/91, and then “evolved independently” through genetic transfer between V. 598

cholerae strains (Blokesch and Schoolnik 2007; Nusrin et al. 2009). 599

600

In conclusion, it is hoped that this research will stimulate new points of investigations 601

in Peru and in other areas where cholera is emergent or reemerging. To begin, future 602

work should consider each dimension of ENSO because each can serve as a potential 603

pathway that links ENSO to disease incidence. Moreover, quantitative studies are 604

necessary to estimate the relationship between each pathway (described in this study) and 605

cholera. For example, in order to better understand the temporal patterns of cholera by 606

region, it may be useful to utilize time series methods, such as wavelet, to identify 607

changes in the climate-cholera relationship across time frequency space (Cazelles et al. 608

2007), including lag effects. Such a task will require researchers to examine the entire 609

record during which cholera was present in Peru (1990/91 to 2002) in order to capture 610

ENSO’s quasi-periodicity. Furthermore, the characteristics of various ENSO events 611

should be explored to understand how an event’s evolution and magnitude (e.g., degree 612

of impact on SST), which is unique to each event, can impact transmission. It may 613

explain why cholera did not emerge during the second strongest event of the century 614

which occurred in 1982/83 or a moderate event in 1986/87, where health impacts were 615

reported in Peru (Gueri 1984). Equally important is the necessity to consider the 616

modifying effects of non-climatic factors, which may also address cholera emergence and 617

transmission questions in Peru. These factors include social variables, such as 618

socioeconomic status and infrastructure (Sasaki et al. 2009; Emch et al. 2010; Mariet al. 619

28

2012), immunity, which influences biological susceptibility (Koelle et al. 2005; Rinaldo 620

et al. 2012), and human migration, which enables connectivity between infected and 621

susceptible populations (Koelle et al. 2005; Mari et al. 2012). 622

623

Acknowledgments. 624

This study was supported through grants at the following institutions at Michigan State 625

University: Department of Geography, Department of Philosophy (Ethics and 626

Development Specialization), Center for Latin American and Caribbean Studies, and the 627

Graduate School. Support was also provided by CCB in Boulder, CO. Special thanks to 628

Ing. Norma Ordinola, University of Piura (Private), Ing. Grover Otero, Proyecto Chira-629

Piura, Dr. Elsa Galarza, University of Pacifico, Joanna Noelia Kamiche Zegarra, 630

University of Pacífico, and Dr. Luis Miguel Castrov V. for facilitating fieldwork in Lima 631

and Piura. We also thank all the institutions who provided data and documents in Peru 632

including MINSA in Lima and Piura, INEI in Piura, and Dr. Ana I. Gil (National Institute 633

of Nutrition Research). We also thank New College of Florida for providing the space to 634

complete this article. Lastly, we acknowledge Dr. Lino Naranjo Díaz (MeteoGalicia) and 635

Dr. Kim Knowlton (NRDC) for their comments and expertise on the first drafts. 636

637

638

639

640

641

642

29

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1090

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1093

1094

1095

1096

1097

49

List of Figures 1098

FIG. 1. Map of Niño Regions. Source: NOAA 1099

(http://www1.ncdc.noaa.gov/pub/data/cmb/enso/Niño-regions.gif ). 1100

1101

FIG. 2. Physical map of Peru highlighting 3 departments: Lima (central coast), Loreto 1102

(north jungle) and Piura (north coast, discussed in Section 5c). Sources: University of 1103

Piura (Private), Peru and Nature Earth (http://www.naturalearthdata.com/). 1104

1105

FIG. 3. Cholera cases (suspected and confirmed) by month for each year from 1993 to 1106

1998 in the Departments of Lima (a) and Loreto (b). Source: General Office of 1107

Epidemiology, MINSA, Lima, Peru. 1108

1109

FIG. 4. Monthly SST anomalies (°C) in 3 Niño regions (1+2, 3.4 and 4) are plotted in 1110

relation to monthly cholera cases (suspected and confirmed) in Peru from 1990 to 1992. 1111

SST anomalies are based on the period 1971-2000. See Table 1 for ENSO events (a) to 1112

(d). Sources: General Office of Epidemiology, MINSA, Lima, Peru and NOAA 1113

(http://www.cpc.noaa.gov/data/indices/). 1114

1115

FIG. 5. Cholera cases (in hundreds) and rainfall (mm in hundreds) for January to April 1116

for 1991 to 2000 at the Miraflores meteorological station (5.17°S, 80.6°W; 30 msnm) in 1117

the subregion of Piura, Peru. Sources: MINSA, Piura and University of Piura (Private), 1118

Peru. 1119

1120

50

1121

Table 1. Listings of El Niño and La Niña events from 1990 to 1992 as defined by SSTA 1122

exceeding ±0.5°C threshold. Each qualifying event is given along with the Niño region, 1123

phase and start and end dates. 1124

1125

Event Region Phase Begin End Duration

(a) Niño 4 El Niño Jul-90 Aug-92 26

(b) Niño 1+2 La Niña Jul-90 Dec-90 6

(c) Niño 3.4 El Niño May-91 Jul-92 15

(d) Niño 1+2 El Niño Nov-91 Jun-92 8

1126

1127

1128

1129

1130

1131

1132

1133

1134

1135

1136

1137

1138

1139

1140

1141

51

1142

FIG. 1. Map of Niño Regions. Source: NOAA 1143

(http://www1.ncdc.noaa.gov/pub/data/cmb/enso/Niño-regions.gif ). 1144

1145

1146

1147

1148

1149

1150

1151

1152

1153

1154

1155

1156

1157

1158

1159

52

1160

FIG. 2. Physical map of Peru highlighting 3 departments: Lima (central coast), Loreto 1161

(north jungle) and Piura (north coast, discussed in Section 5c). Sources: University of 1162

Piura (Private), Peru and Nature Earth (http://www.naturalearthdata.com/). 1163

1164

1165

1166

1167

1168

1169

1170

53

1171

FIG. 3. Cholera cases (suspected and confirmed) by month for each year from 1993 to 1172

1998 in the Departments of Lima (a) and Loreto (b). Source: General Office of 1173

Epidemiology, MINSA, Lima, Peru. 1174

(a)

(b)

54

1175

FIG. 4. Monthly SST anomalies (°C) in 3 Niño regions (1+2, 3.4 and 4) are plotted in 1176

relation to monthly cholera cases (suspected and confirmed) in Peru from 1990 to 1992. 1177

SST anomalies are based on the period 1971-2000. See Table 1 for ENSO events (a) to 1178

(d). Sources: General Office of Epidemiology, MINSA, Lima, Peru and NOAA 1179

(http://www.cpc.noaa.gov/data/indices/). 1180

1181

1182 1183

1184 1185 1186

1187

1188

1189

-1.5

-1

-0.5

0

0.5

1

1.5

2

2.5

J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D

1990 1991 1992

SS

TA

(°C

)

0

10000

20000

30000

40000

50000

60000

70000

80000

90000

100000

Cho

lera

Case

s

Cholera Niño 1+2 Niño 3.4 Niño 4

Epidemic

begins

First

possible

cases(a)

(b)

(d)

(c)

55

1190

FIG. 5. Cholera cases (in hundreds) and rainfall (mm in hundreds) for January to April 1191

for 1991 to 2000 at the Miraflores meteorological station (5.17°S, 80.6°W; 30 msnm) in 1192

the subregion of Piura, Peru. Sources: MINSA, Piura and University of Piura (Private), 1193

Peru. 1194

1195

1196

1197

1198

1199

1200

0

1

2

3

4

5

6

7

8

9

0

20

40

60

80

100

120

J FMA J FMA J FMA J FMA J FMA J FMA J FMA J FMA J FMA J FMA

1991 1992 1993 1994 1995 1996 1997 1998 1999 2000

Rain

fall

(mm

in h

undre

ds)

in P

iura

(Jan

-Apr)

Chole

ra c

ases (

in h

undre

ds)

in P

iura

(Jan

-Apr)

Cholera Rainfall