Ecology of Zoonotic Transmissions: The Impact of Bos taurus indicus Fertilizer on the Health of Malagasy Farmers

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Photo Courtesy of Rachel Lordahl

By Zuri S. Dawkins

Central ValBio

Ranomafana National Park, Madagascar

Undergraduate Program in Anthropology and Biology, Stony Brook University

Madagascar Institute for the Conservation of Tropical Environments (MICET)

Contact Info: Zuri.Dawkins@stonybrook.edu

ABSTRACT

Emerging infectious diseases in livestock pose a huge threat to human health, animal efficiency and biodiversity. Zoonotic diseases are highly contagious diseases that spread amongst animals and humans via bacteria, viruses and parasites. They are especially prevalent in third world countries that do not have access to the necessary antibiotics

to help prevent such outbreaks. This study takes place in Ranomafana, Madagascar, where much of the indigenous population makes their living by farming crops. Rice- fields are especially a huge part of Madagascar culture, as they offer food and income to many families. Bos taurus indicus (a cattle breed of Madagascar, formerly known

as Zebu) are used in the plowing process and their manure is used as fertilizer for many farmers. High contact with fecal matter may be the cause of seasonal zoonotic illnesses within the Ranomafana area. Two different communities: Ambatovaky and Alakamisy Ambohimaha, each representing the Betsileo ethnic group, were selected and roughly

20 households from each were surveyed. The top five zoonotic symptoms in accordance with the CDC were used to assess indication of zoonotic illness. Surveys were used to examine correlations amongst the months of fertilizer usage and the time of year farmers expressed zoonotic symptoms. A strong correlation was found between the months of fertilizer usage and the months Malagasy farmers indicated signs of zoonotic symptoms. This study could be used to obtain world health statistics as well as offer insight on improving Malagasy farming techniques and animal-to-human hygiene.

 

Key words: zoonotic transmissions; agricultural fertilizer; Zebu; rice-fields; Malagasy farmers

 

BACKGROUND

Zoonotic diseases and symptoms

Emerging infectious diseases in livestock pose a threat to human health, animal efficiency and biodiversity. Zoonotic diseases are highly contagious diseases that spread between animal and humans via bacteria, viruses and parasites. These diseases can be transmitted from human to animals and vice versa. Zoonoses are threats to the community health, so finding ways to manage and control the spread of these diseases are a primary goal of public health. Shigellosis is an infectious disease caused by bacteria called Shigella. It is transmitted through feces-contaminated food or water. Its symptoms include: diarrhea, fever, and stomach cramps starting within a few days after being exposed to the bacteria.  In addition, Escherichia coli (or E. coli) are bacteria that normally live in the intestines of humans and animals and are commonly found in the manure of cattle. Although most strains are harmless, several are known to produce toxins that can cause diarrhea (Washington State Department of Health. Web). In accordance with the World Health Organization, about 75% of the new diseases that have affected humans over the past 10 years have been caused by pathogens originating from an animal or from products of animal origin. Many of these diseases have the potential to spread through various means over long distances and to become global problems (WHO).

 

Many zoonotic diseases that spread from livestock to humans deal with the handling of manure and unsanitary farming practices. The use of contaminated manure as a source of fertilization of crops poses a huge threat to food and water contamination as well as human and animal health. The FDA in the U.S. has specific regulations on the use of manure and composts. However, the regulations on the use of manure in Madagascar are unclear. This study helps elucidate how sanitary and effective crop planting is beneficial on the health of farmers in Madagascar and explores effects on animal health and overall community health.

 

Rice Farming Process

In Madagascar, farmers usually plant two times a year. The first planting season is from August to October and farmers cultivate rice in the months of December to February. Typically, it takes about 4-5 months to obtain the rice. During this time rice is only available in small amounts (maybe 10 bags of rice per farmer). Farmers use water from their local dam on their rice fields. After cultivation they sell the rice in the market to buy more NPK fertilizer to use for the second planting season. The second planting season is from October to November with cultivation months from March to April. This time the water used for cultivation comes from  rain and farmers cultivate larger amounts of rice during this season. Rice farming is very important as Madagascar ranks 5th in the world in terms of per capita consumption –136 kg/year, or 0.375 kg per person per day (Laulanié 183). Although animal manure is used more heavily as a fertilizer because it is cheap and easier to obtain, most farmers combine NPK fertilizers and manure to nurture their crops. Chemical fertilizer use in Madagascar is one of the lowest in the world…The low fertilizer use is largely explained by economic reasons. The ratio of the price of one kilogram of fertilizer over the price of a kilogram of paddy in rural areas hovers over time above 2 (Minten and Dorosh 4). Frequent use of cattle manure during planting seasons increases bacterial contact.

 

Ranomafana – Betsileo people

Ranomafana is a town in Madagascar; it belongs to the Vatovavy-Fitovinany region.

60% of the population consists of farmers with rice and banana serving as the cash crops. Pineapple, cassava and other vegetables are regularly planted as well. The Betsileo people are considered the best farmers of Madagascar as they build rice fields on the slopes of hills (Wild Madagascar, Web) and maintain very efficient farming techniques. Ambatovaky and Alakamisy Ambohimaha are communities within and surrounding the Ranomafana area. Ambatovaky is closer the the Ranomafana National Park and consists of many farmers living in a rural area. Alakamisy is further out mainland and has a larger population and  has its own water dam for community use.

 

Agricultural fertilizers

There are three main types of agricultural fertilizers: animal manure,  compost, and green manure. Manure is an organic matter that is used for fertilization in agriculture and it is usually obtained after decomposition of organic products like cow-dung, which replenishes the soil with essential elements and nutrients (such as nitrogen). Compost consists of decomposed remnants of organic materials; usually plants but often include some animal feces. Lastly, green manures are crops grown specifically for plowing (like clover and leguminous plants). Malagasy farmers use animal manure from their Zebu and compost to fertilize their crops. Bacteria in the fertilizers they use can lead to an increase in zoonotic transmissions amongst farmers.  Zebu came to Madagascar via dispersal many years ago and today they are the heart Malagasy culture. Malagasy farmers praise Zebu and farmers are sometimes ranked based on how many Zebu they own. Zebus are essential for plowing rice farms and their fecal matter is often used as fertilizer in the field.

 

INTRODUCTION

Research summary: The impact of Zebu (Bos taurus indicus) fertilizer on the health of Malagasy farmers during rice and vegetable farming periods and its correlation with zoonotic transmissions was studied. The questions addressed are as followed: Are higher health issues in Malagasy farmers correlated to the seasons in which Zebu manure is applied to the rice and vegetable fields? During the seasons of rice cultivation are Malagasy farmers more susceptible to zoonotic illness? Are farmers who use more bags of fertilizer more susceptible to zoonotic transmission than farmers who use fewer bags/have less contact with the fertilizer? Do farmers who wait longer to use fertilizer after animal defecation have higher symptoms than farmers who do not? Do the health records from the local hospital show any correlation with the cultivation months? How can we use this data as a basis of mapping out the rate of how zoonotic diseases spread to implement better hygienic strategies to be used in the field? It was hypothesized that Bos taurus indicus fertilizer usage causes zoonotic illnesses in farmers. The time of year farmers show signs of zoonotic symptoms served as the dependent variable and the time of year farmers use Zebu fertilizer and the amount of Zebu fertilizer farmers use served as the the independent variable. There were two predictions: (1) Farmers will express an increase in zoonotic symptoms and health issues during rice farming and vegetable planting seasons than during non-farming periods and  (2) Farmers who use higher amounts of fertilizer will indicate a higher frequency of illnesses  during periods of usage.

 

METHODS

Materials: 40 Surveys, Gifts for Malagasy farmers (chocolate, tea, candy, pens, soap etc.)

 

Study Site: The three-day data collection via survey questions took place around Ranomafana National Park, Madagascar. The research was conducted during July, which is the coolest month in Madagascar, with mean monthly temperatures around the island ranging from the low 50s °F (low 10s °C) to the high 70s °F (mid-20s °C) (Madagascar 3). Two communities within the Ranomafana area were selected (Ambatovaky and Alakamisy Ambohimaha) and roughly 20 households from each community were surveyed.Each community was representative of the Betsileo ethnic group. The two communities are located near each other but in different areas of Ranomafana National Park. Rainforests are prevalent in this area and during this cool, dry season (May to October), the hauts plateaux (central highlands; which include Antananarivo) can get cold and windy, with freezing showers (Tony and Maureen Wheeler 1). In addition, the two communities have different time periods for farming and crop cultivation but have similar agricultural processes. A total of 38 farmers (23 males and 15 females) and one doctor were interviewed. Farmers were selected randomly based on whoever was working in the field on the day of the study. Farmers were not selected based on gender; male to female ratio was deemed inconsequential for the results of this study. However, selecting farmers by household was not random. Only farmers from different households were surveyed to assess data points for multiple homes in the community. Lastly, one doctor from Ranomafana Hospital was interviewed to give a general census of the time period most farmers come in with symptoms that pertain to most zoonotic illnesses. The top 5 symptoms of zoonotic illnesses were recorded (in accordance with the CDC): Diarrhea, bloody stool, stomach cramps, fever, and vomiting. Farmers were asked what time of the year they normally get sick and if they had any of the five symptoms during their period of illness. These answers were correlated to the months that farmers used fertilizer to nourish their crops.

Survey Approach: Survey questions were translated in Malagasy and formally asked to each farmer of a different household, to assess multiple households for each community. Participants gave oral consent to surveys. In addition, prior to visiting the community, the village king/chief of each area gave permission for our research to be conducted. Day 1 of data collection (Wednesday, August 6th 2014) took place in the Ambatovaky community, where 13 survey questions were asked per household to a total of 16 farmers. Day 2 of data collection (Thursday, August 7th 2014) took place in the Alakamisy Ambohimaha community, where 17 survey questions were asked per household to a total of 22 farmers (Figure 1). Some survey questions were added, changed and translated properly in order to obtain genuine answers to specific questions. The last day (Day 3 – Friday, August 8th 2014) of data collection was held at Ranomafana Hospital, and 5 survey questions were asked to the local doctor to assess a general census of the main seasons farmers come in for zoonotic symptom illnesses.


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Figure 1. Sample survey questions distributed to Alakamisy Farmers

 

Statistical Approach: Microsoft Excel was used to compile data, create graphs and  tables, and analyze any correlations amongst the collected survey answers.

 

RESULTS

Survey Results: 38 individuals were surveyed based on the symptoms they normally express when they are sick. Anyone with zoonotic symptoms was assessed as sick for the purpose of the study (Figure 2). High levels of fever were expressed by 26 out of 38 farmers.. Diarrhea and stomach cramps followed closely as  zoonotic symptoms expressed when farmers were sick. Farmers expressed symptoms in other aspects such as backaches, eye problems, foot problems, heart problems, and flu which were classified as non-zoonotic symptoms. Farmers had more than one symptom when ill, so the graph represents the number of individuals with each symptom and not merely a single farmer.

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Figure 2: Distribution of Farmers Expressing Symptoms Number of Individuals with zoonotic and non-zoonotic symptoms. Sample size: 38. Farmers may represent more than one bar graph because they expressed more than one symptom on the chart.

 

When surveying the farmers one question was asked: Do you think the fertilizer made you sick? 95% of farmers who answered did not think the use of fertilizer made them sick. However, when asked what symptoms they express when they are sick, 29/38 or 79% of individuals indicated that they had zoonotic symptoms when they were sick,with 45% (nearly half) of those farmers stating that they had these symptoms in the same months they used the fertilizer (see Figure 3 below).

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Figure 3: Percentage of Farmers Surveyed that Show Signs of Zoonotic Symptoms. The first pie chart indicates the percentage of farmers who said that they exhibited any of the five zoonotic symptoms when they were sick. The second pie chart indicates the percentage of farmers that actually expressed zoonotic symptoms during the months they used fertilizer on their crops in their surveys. N/A: the farmer did not indicate months of illness. Sample size: 38.

 

The initial prediction was that farmers would express an increase in zoonotic symptoms and health issues during rice-farming and vegetable-planting seasons than during non-farming periods. This was only true for one of the villages that was surveyed (Alakamisy). Many of the farmers became sick and exhibited zoonotic symptoms at the  time  they were planting rice and using animal manure for fertilizer. However, the people of Ambotovaky were not becoming sick during the months  they were using fertilizer. Instead, they expressed illnesses in the months of January to February, months after they have planted their crops (see Figure 4 below). This is the cyclone season and the heaviest period of rainfall and climate destruction. In addition, Alakamisy people plant rice two times a year because they have a local water dam. Ambotovaky people usually plant rice once a year (twice if the weather permits) since they do not have access to the water dam.

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Figure 4: Number of Farmers that use Fertilizer on their Crops vs. the Percentage of Farmers Who Are Sick in These Months.

 

The second prediction was that farmers who use higher amounts of fertilizer during the time periods in which they plant crops would indicate a higher frequency of illnesses per year. The correlation test calculated a value of -0.221. The value, although closer to 0 than -1, is still a negative correlation and indicates the opposite of the initial prediction. Instead, the higher amounts of fertilizer used generally caused a decrease in the frequency of illnesses over the year.


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Figure 5: Amount of Bags of Fertilizer Used As Compared to Frequency of Illness. A correlation test on the effects of the amount of exposure to fertilizer on farmer health. Data points represent the total number of bags used in that month by all of the farmers who plant during those months. One bag is equivalent to 50 lbs. Frequency of illness data point represent only zoonotic illnesses. Sample size: 38.

 

Hospital Results

Five questions were asked to the local doctor at Ranomafana Hospital. Two main questions were relevant to my predictions. They are as follows:

 

  1. What time of year (months) do people come in with these symptoms:?
  •    Diarrhea?
  •    Bloody Stool?
  •    Stomach Cramps?
  •    Fever?
  •    Vomiting?
  1. What illness(es) do most people come in with (dominant illness in Ranomafana)?

 

Although there were no health records, results from the doctor indicated that farmers came in for treatment related to diarrhea during the rainy season (November through February). Treatment related to bloody stool and stomach cramps were generally year round with most individuals coming in for stomach cramps because of eating habits or consumption of too much tokogasy (a Malagasy alcoholic beverage). In addition, farmers typically came in for fever and vomiting treatment during the rainy and humid season (November through April). The most common illnesses most farmers came in for treatment were for fever, flu, and diarrhea (including belly aches).

 

DISCUSSION

Interpretations: The sample size within the study was very small (only 38 individuals). Therefore, it is hard to conclude accurately that the Zebu fertilizer is the main reason some Malagasy farmers are expressing zoonotic symptoms during the months that they are planting, but it can be said that usage and direct contact with Zebu fertilizer is one of many factors as to why these farmers exhibited these symptoms.

 

Results from the experiment suggest that the first prediction was proven true for only one of the villages: Alakamisy. Farmers were expressing high amounts of zoonotic symptoms in the same months they were using Zebu fertilizer. The results gathered from the Ambatovaky people, on the other hand, did not show the same correlations. Ambatovaky people could be suffering from illnesses as a result of a range of other causes, especially since cyclone occurrence is higher in the month of February than any other month. During the cyclone period, the weather is very unpredictable, making it extremely hard to grow crops for food and thus many people are left to starve. Farmers could possibly be getting sick from water contamination (since this time period is the rainy season) or a decreased supply of food because of cyclone effects. Although it cannot be determined from this data that Ambatovaky farmers are getting sick from zoonotic bacteria in the fertilizer they use, it can be said that there is a chance that the people are getting sick from other ways of zoonotic transmission, such as water contamination. Water contamination (which consists of many parasites) could also be the cause of high zoonotic illnesses in the farmers of Alakamisy.

 

The results for the second experiment reject the second hypothesis. Farmers who used more bags of fertilizer did not express higher frequencies of illnesses throughout the year; instead the two variables were negatively correlated. The more bags of fertilizer the farmers used the less frequently they expressed illnesses.

 

Lastly, results from the local hospital indicated that farmers were expressing zoonotic symptoms. In fact, two out of the three most common illnesses in Ranomafana (according to Ranomafana Hospital Doctor) are symptoms of zoonotic illnesses (fever and diarrhea).

 

There are many other reasons why farmers could be getting sick during the months that they are using fertilizer. Food is scarce at this time and so is money, so many homes go without food and thus the people receive little nutrition. In addition, farmers could be getting sick from other zoonotic diseases not associated with the fertilizer such as malaria and parasitic illnesses acquired in the fields when walking barefoot. This study is a good platform to educate farmers on health and agricultural hygiene, so that they can understand the necessities of implementing better sanitary farming practices to care for their health as well as the health and well being of their Zebu.

 

Sources of Error: There were some sources of error that could have resulted in biases in the data that were collected. For instance, the research took place in Madagascar, where there are certain terminologies in English that do not translate well into Malagasy. Therefore, translating the questions based on what was being asked was difficult at times and several questions had to be changed and simplified. The language barrier caused some miscommunication and it was the job of the Malagasy research assistant to ask the exact questions written on the surveys. Human error was also evident as it had to be assumed that the farmers’ answers were truthful and honest. Some farmers could not recall the months during which they usually get sick, so many times the answers they provided were merely estimations. Therefore, these estimations could have biased the results of the study. In addition, the Ranomafana Hospital had no health records of the patients  they see, so the information the doctor provided was assumed to be true and honest to the best of her ability.

 

Findings: Many of the farmers keep their manure in an outdoor room and allow the fertilizer to pile up over time. It was not a point of contention for the study, but one can infer that it should not be too far from the farmland. This could also cause zoonotic transmissions, allowing bacteria to fester. Some farmers mix the animal feces within their compost as well. Also, many farmers do not wear shoes or proper footwear when planting, and many times their feet go bare as they plant and plow the rice fields. This allows for increased parasite infections. Veterinarians are scarce in the Ranomafana area, and although the natives take good care of their cattle, they still may have parasitic infections or need annual check-ups that are not at their dispersal. Some farmers in the society do not go to the hospital or doctors when they are ill. Instead they find other matters or visit the medicinal man in their community for alleviation of their illnesses. Lastly, many of the farmers may be immune or less severely affected by the symptoms of zoonotic illnesses due to the fact that they reside in an underdeveloped country. Thus, it might be expected that their bodies have developed strength and resilience pertaining to certain health issues.

 

Future Studies: Many steps can be taken in order to assess the significance of different confounding variables, such as asking survey questions amongst two different ethnic groups and comparing the differences; interviewing more than two communities in the Ranomafana area to assess an accurate significance; and visiting the clinics and the hospitals that the farmers go to and interviewing different doctors for health records. Also, in the future tests should be done on the Zebu and the owner (farmer) to confirm how healthy individuals are in actuality. These studies could also be compared amongst different regions of Madagascar as well as different countries. This test shows that there is an issue surround the health of the community with regards to infectious diseases and there is a huge need for public health in underdeveloped countries to control and prevent the spread of harmful bacteria and infectious disease.

 

ACKNOWLEDGEMENTS

  • Dr. Cassidy Rist, DVM
  • Lazasoa Rehodo (Education Assistant at CVB – Malagasy Research Assistant)
  • Ralazampirenena Claude Jacquot (Student with TEAM Project – Statistical and Survey

Analysis Assistant)

  • Dr. Patricia Wright
  • Dr. Tharcisse Ukizintambara
  • Gena Sbeglia
  • Franck Rabenahy

Special Thanks to the entire Central ValBio staff, the people of Ambatovaky and

Alakamisy, Ranomafana Hospital, Ange Raharivololoniaina, Elizanjara, Rachel Lordahl

& Stony Brook University

 

LITERATURE CITED

 

Bublitz DC, Wright PC, Bodager JR, Rasambainarivo FT, Bliska JB, et al. (2014) Epidemiology of Pathogenic Enterobacteria in Humans, Livestock, and

Peridomestic Rodents in Rural Madagascar. PLoS ONE 9(7). Web

 

Butler, Rhett. Peoples of the Central Highlands of MADAGASCAR. Country Studies

Madagascar – Area Handbook program of the U.S. Department of the Army. August

  1. Copyright 2004 – 2012. Web

 

Center for Disease Control and Prevention. Zoonotic Disease: When Humans and

Animals Intersect. Mar. 2014

 

De Laulanié, H. Intensive Rice Farming in Madagascar. TROPICULTURA, 2011, 29,

3, 183-187

 

Diseases Found in Cow Manure.GardenGuides. N.p., n.d. Web. “E. Coli.”: Washington State Dept. of Health. N.p., n.d. Web.

“Madagascar.” Encyclopaedia Britannica. Encyclopaedia Britannica Online Academic

Edition. Encyclopædia Britannica Inc., 2014. Web.

 

Minten, Bart and Dorosh, Paul with Dabat, Marie-Hélène; Jenn-Treyer, Olivier; Magnay, John and Razafintsalama, Ziva. Rice Markets in Madagascar in Disarray: Policy Options for Increased Efficiency and Price Stabilization. Africa Region Working Paper Series No. 101. September 2006

 

Minnesota Department of Health, Acute Disease Investigation and Control

Common Zoonotic Diseases from Farm Animals. Dec 2012

 

Pelzer, Kevin D. and Currin, Nancy D.V.M. Zoonotic Diseases of Cattle. Virginia

Cooperative Extension. Veterinary Extension Publication Specialist, Virginia Tech. May

2009

 

Stephen, Craig, Harvey Artsob, William R. Bowie, Michael Drebot, Erin Fraser, Ted Leighton, Muhammad Morshed, Corinne Ong, and David Patrick. Perspectives on emerging zoonotic disease research and capacity building in Canada. Can J Infect Dis Med Microbiol. 2004 Nov-Dec; 15(6): 339–344. National Center for Biotechnology Information. U.S. National Library of Medicine, 25 Apr. 0006.

 

Tony and Maureen Wheeler “Madagascar.” Weather in Madagascar. Lonely Planet N.p., n.d. Web.

 

Shigellosis.” Resources – Notifiable Conditions. N.p., n.d. Web. “Veterinary Public Health (VPH).” WHO. N.p., n.d. Web.

 

REFERENCES

 

American Journal of Primatology: http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)

10982345/homepage/ForAuthors.html

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