Manure management practices among 119 Morogoro urban and peri-urban cattle keepers.
Urban and peri-urban livestock farming has been expanding in recent decades due to high demand for animal proteins to feed the growing urban population. The increase in number of livestock and livestock keepers has led to increased manure production in a shrinking space. This chapter evaluates the risks of transmission of manure-borne pathogen between cattle, humans and the environment in urban and peri-urban areas. Cattle and manure management practices, government directives, the presence of zoonotic pathogens and risk of bacteria transmission were assessed by observations, interviews, bacteria isolation and characterization and statistical modeling. Cattle are kept under intensive and extensive systems. Different techniques are used to collect, convey, store and dispose manure, all of which lead to direct contact with humans. The prevalence of diarrheagenic Escherichia coli in cattle and water was 2.2% (95% CI: 0.99–3.67) and 0.5% (95% CI: 0.025–2.44), respectively. There was transmission of bacteria between cattle, humans and the environment in 52% of clusters. Cattle and manure management practices expose humans, livestock and the environment to risk of infection or contamination. Holistic approach can be adopted in this scenario to attain one health status and improve urban and peri-urban livestock contribution to community livelihood simultaneously.
- manure management
- pathogen transmission
- system thinking
- one health
Urban areas are city areas characterized by a dense human population of mixed age, sex, family and household structure, ethnic, cultural, religious diversity, educational and income levels, and high built-up area with technological and economic advancement. Rural areas, on the other hand, are open broad areas of land located far from towns and cities, which are composed of extensive bushes between large crop fields and livestock herds and sparse housing and population density. Between the urban and rural settings lies peri-urban zone whose population, livestock, crops and land use features are influenced by the proximate interface. Part of peri-urban area adjacent to urban area has features resembling urban features, while its other side assumes the rural characteristics. There is no distinct line separating the peri-urban from urban and rural settings, but a slow zone of change . The gradual transition from peri-urban to urban setup is moving constantly away from city center toward the rural direction due to persistent urbanization pressure, especially in developing countries.
Urban and peri-urban livestock farming is expanding in developing countries primarily due to high demand for protein of animal origin to feed the rapidly growing urban populations, but also to generate income of livestock keeping households . It is also a diversification tactic to spread livelihood risks in adverse situations . Some urban and peri-urban dwellers continue to keep livestock to maintain their rural cultural values . The expansion of urban and peri-urban livestock farming, which is reflected as an increase in number of both the livestock and households involved in keeping livestock, and rapid urban human population growth has increased the chance of contact between humans, animals and manure. Urban areas of Morogoro in Tanzania, for example, had a cattle population of 2618 in 1996 , which almost doubly increased to 4170 in 2006 . By 2008, the cattle population in Morogoro urban was 19,099, and among them, 4425 were dairy cattle . This cattle population hiked up to 49,625 in 2012 . Rapid urban population growth is primarily caused by influx of people from rural areas either as migrants or as commuters [1, 9]. For instance, Tanzania's annual population growth rate between 1988 and 2002 was 3% with the urban population size increasing from 18% in 1988 to 23% in 2002 . Moreover, population size and growth in rural and urban areas of Morogoro region from 2002 to 2012 show that the rural population grew by 23.7% from 1,279,513 in 2002 to 1,582,434 compared to 34.2% growth in urban population from 473,849 in 2002 to 636,058 in 2012 . In this region, the general population density changed from 24 persons per square kilometer in 2002 to 31 persons per square kilometer in 2012 . As a result of increased human and animal density, the chance of contact between humans and livestock has increased. The growth in animal population and concomitant increase in manure production, in shrinking space separating humans, livestock and manure, require appropriate livestock and manure management practices taking into account that livestock harbors zoonotic pathogens .
Four decades ago, before the expansion of urban and peri-urban livestock farming, free open communal cattle grazing system required minimal effort to manage manure [3, 13]. Cattle freely grazed during daytime and were confined during the night for security. Most manure was left scattered everywhere except for a small amount which was applied on crop fields [3, 14]. To date, the manure management practices have changed to adapt to densely populated areas where the space separating humans from animals and their wastes has decreased. A question arises: does this change consider prevention of animal and human from pathogen exposure as well as environmental contamination? This chapter describes assessment of manure management practices and risks of contact and transmission of cattle manure-related zoonotic pathogens between cattle, humans and the environment in urban and peri-urban areas of Morogoro region of Tanzania. This report forms a basis for developing strategies to improve urban and peri-urban livestock farming practices in order to safeguard human, animal and ecosystem health in settings similar to study area.
2. Exploration of animals-humans-environment interaction
Most of the people who keep cattle in urban and peri-urban areas also keep other livestock such as goats and chicken. Members of livestock keeping households share premises with livestock. In this community, livestock keeping households are randomly mixed with households which do not keep livestock. There is no tangible demarcation between livestock keeping households and non-livestock keeping households, and hence, the two types of households are in close contact. A total of 119 households keeping cattle, randomly selected, were willingly enrolled for the study in urban and peri-urban areas of Morogoro, Tanzania. Each cattle keeping household was paired to a non-cattle keeping household selected from any direction within a radius of 100 m for purpose of comparison. This pair was regarded as a cluster. Assessment of the interaction between cattle, humans and the environment within and between clusters involved field visits in order to make observations and interview household representatives about livestock and manure management practices. Questionnaire to cattle keeping households inquired about herd characteristics and management, manure management practices, awareness on zoonotic health risks and constraints to livestock farming in urban and peri-urban areas. Observations were made to top up and confirm the information gathered from the questionnaire. Details of labor division, herd composition and size, animal housing and feeding, herd health management, means and frequency of manure collection, storage and disposal were obtained at household level. Questionnaires to non-cattle keeping households enquired about attributes which may contribute to contact between humans, cattle and manure. Moreover, District Livestock Officers were interviewed about monitoring of manure handling practices in their respective areas of jurisdiction and were asked to present documents guiding livestock and manure management. This cross-sectional study was carried out from February 2010 to February 2012.
Cattle feces, human stool, soil and water samples were collected from each participating household for isolation and characterization of bacteria to check for the presence of pathogens and evidence of transmission between cattle, humans and the environment. In this particular study,
Ethical clearance was approved by Sokoine University of Agriculture Ethical Committee to handle animals and animal samples. Approval was also obtained from the Tanzania National Institute for Medical Research (NIMR) Ethical Board (NIMR/HQ/R8a/Vol. IX/927) to handle and process human sample. All conditions for research approval were observed throughout the study.
3. Cattle and manure management practices
Observations and face-to-face interviews conducted during field visits to 119 households keeping cattle generated data which were analyzed by descriptive statistics such as means, frequencies and cross-tabulations by using SPSS 15.0. Information about herd characteristics and management, manure management practices and awareness on cattle manure-related zoonotic pathogens was obtained from the cattle keepers and Livestock Officers.
From observations and interviews, a total of 806 cattle were kept by study participants (minimum = 1, maximum = 36, mean = 7, median = 5, SD = 5.85), 95.8% of whom also kept animal species other than cattle in same residential premises. These animal species, with percentage of participants keeping these species in brackets, include chicken (80.7%), dogs (62.2%), goats (50.4%), pigs (27.7%), ducks (23.5%), cats (21.9%), sheep (10.9%), guinea fowls (9.2%), turkeys (5.9%), guinea pigs (1.7%), rabbits (1.7%) and monkey (0.8%). Cattle and manure management practices were carried out either by family members (46.2%) or by hired laborers (53.8%). Most cattle houses (71.4%) had concrete floor and the rest (28.6%) had floor made of earth. It was observed that majority of cattle houses (84%) had roofs and 16% were open cattle “boma.” Cattle kept in earth floor houses with open or broken roof stayed on mud during rainy season. Three out of 119 respondents (2.5%) put grass on the floor of cattle house as bedding material, one of them had a house with earthed floor. All respondents kept their cattle in a confinement near to their residence for security reasons. Cattle were fed by “cut and carry” method under intensive system (47%) or were allowed to go around foraging (53%) where they mixed with livestock from other herds. There was sharing of water sources between cattle and humans. Free range cattle (40.3%) used surface water such as rivers, ponds and wells, while intensively kept cattle (59.7%) were provided water from taps also serving the people .
Overnight confinement of cattle resulted into manure accumulation which necessitated collection and storage/discard. Various methods were employed to collect, convey and store or discard manure. These included uses of utensils like spade, bucket or plastic bags, use of water splash and use of bare hands. Manure was collected by bare hands by a few respondents where there was direct contact with the manure. However, the majority of respondents used utensils such as spades, hand hoes and rakes to collect manure into a pile within the cattle house. Some respondents used a water hose to collect manure (Table 1). Manure was removed from cattle house at different rates per day, week or month to storage or disposal site by using utensils (plastic bags, buckets, raw hides, spades and hand hoe and wheelbarrow), bare hands or water. The use of rubber boots was an observed practice by less than a half of the respondents, while the remaining fraction wore ordinary shoes, e.g., sandals or were barefooted while handling manure (Table 1). In all these different manure collection or conveyance methods, people did not use any protective measures such as special clothes or gloves and were observed to have direct skin contact with manure. A large proportion of respondents stored manure into piles before disposal as fertilizer or waste, whereas a few respondents threw fresh manure from cattle house direct into the surroundings. Most cattle keepers disposed manure within a radius of 10 m from their residential houses, especially those with land area of more than 1000 m2. Respondents who did not spread manure on land opted for burning or giving it away to friends in plastic bags. Allowing effluent from cattle house to leach into immediate land was a common practice among cattle keepers although a few cattle keepers directed the effluent into a pit (Table 1).
|Manure disposal method||Spread on land||108 (90.8)|
|Not spread on land||11 (9.2)|
|Means of manure collection||Hand picking||5 (4.2)|
|Use of utensils||112 (94.1)|
|Water splash||2 (1.7)|
|Frequency of manure collection||Once a day||72 (60.5)|
|More than once a day||19 (16.0)|
|Means of manure conveyance||Hand picking||3 (2.6)|
|Use of utensils||115 (96.6)|
|Water splash||1 (0.8)|
|Use of rubber boots||Yes||70 (58.8)|
|Manure treatment||Heaping||99 (83.2)|
|Direct spread on land||20 (16.8)|
|Manure disposal distance||Within 10 m from residence||83 (69.7)|
|Outside 10 m from residence||36 (30.3)|
|Effluent treatment||Direct spread on land||95 (79.8)|
|Use of pit||24 (20.2)|
|Household area||>1000 m2||87 (73.1)|
|≤1000 m2||32 (26.9)|
Out of 119 respondents, 5% reported to have heard about manure-associated pathogens which can infect human. There were 125 responses to problems related to manure management which respondents encounter. Out of these 125 responses, 77 (61.6%) said they encounter no problem, while 15 (12%) responses reported that poor infrastructure impedes manure management practices. Lack of working facilities such as utensils and transport was reported in 13 (10.4%) responses as one of the problems cattle keepers face, whereas land scarcity appeared in 6 (4.8%) responses. Health problems related to respiratory tract, injuries and foot rot to manure handlers were mentioned in 5 (4%) responses, same as for the presence of poor cattle housing facilities. Odor and water scarcity were each mentioned in 2 (1.6%) responses as among problems of manure management practices in urban and peri-urban areas of Morogoro.
During the interview, Livestock Officers presented documents such as “Environmental Sanitation By-Laws” and “Animals in Urban areas By-Laws” which give directives on animal keep in the area and how to deal with wastes including manure. From interviews and the documents, the guideline which allows maximum herd size of four cattle per herd in urban area does not give area requirement specification and is not observed, and cattle manure is regarded by the by-laws and treated like any solid household waste . It was observed that cattle keeping households are randomly distributed among non-cattle keeping households and there are no preconditions for a household to start keeping cattle. Anybody can start a herd of cattle anywhere in urban and peri-urban areas of Morogoro at any time.
The current manure management practices differ from those methods used a few decades ago in both the actual practices and resource base available which is shared between humans, animals and manure. Increased manure production in populated urban and peri-urban areas has resulted into the problems mentioned by cattle keepers. Some of these problems such as land scarcity odor and increased flies population have been previously reported to be due to exclusion of livestock farming during urban and peri-urban land use planning . Increased manure production in a shrinking space has forced cattle keepers to collect, convey, store and finally dispose manure. Diverse cattle and manure management practices are determined by customs, convenience and availability of resources including land and equipment. Some farmers said that they keep cattle and handled the manure by the same methods since childhood; others opted for a particular cattle and manure management practice because it was easy to execute. Generally, there was direct contact between humans, cattle and manure and there was environmental contamination by fresh manure. In this scenario, humans, animals and environment are exposed to manure-related pathogens.
4. Pathogens in cattle, humans and the environment
Sample size of 100 clusters was calculated as previously described . Face-to-face interviews were conducted to cattle keeping household members about cattle and manure management practices. Interview was also conducted to cattle keeping household neighbors who do not keep cattle about possible contact with cattle and manure. Individual fecal samples from 446 cattle, 100 stool samples from individuals keep cattle and 100 who do not keep cattle, 200 soil and 200 water samples from sources within homesteads were collected for bacteria isolation.
Somatic antigen O and flagella antigen H on diarrheagenic
Phenotypic activity of virulence genes was assessed on Vero cell monolayers to test for cytopathic effects using protocol formerly described .
For non-typhoidal Salmonella spp. isolation, 1 ml of the sample suspension was enriched by overnight incubation in selenite fecal broth at 37°C. The bacteria growth was subcultured on Salmonella-Shigella agar at 37°C for 24 h. Colorless colonies with a black center were biochemically tested by urease and lysine carboxylase tests. Urease-negative and lysine carboxylase-positive colonies were tested against Salmonella polyvalent agglutinating sera (REMEL30858201 ZC02—LOT 820883) and serotyped by Kauffmann-White M03-03-001 method at Danish Institute for Technology (DTU).
|Cattle||O157:H7||VTEC||vtx2, eae, ehxA and astA|
|Cattle||O157:H7||VTEC||vtx2, eae, ehxA and astA|
|Cattle||O157:H7||VTEC||vtx2, eae, ehxA and astA|
|Cattle||O157:H7||VTEC||vtx2, eae, ehxA and astA|
|Cattle||O+:H16||VTEC||vtx1 and vtx2|
|Cattle||O113:H21||VTEC||vtx1 and vtx2|
|Cattle||O142:H34||EPEC||eae, EAF and bfpA|
|Water||O142:H34||EPEC||eae, EAF and bfpA|
|Cattle||O+:H-||A/EEC||eae ehxA and astA|
The prevalence of
The VTEC strains contained
Isolation of diarrheagenic
5. Transmission of bacteria between cattle, humans and environment
The study on transmission of bacteria involved 100 clusters, and each cluster was formed by a pair of a cattle keeping household and a neighboring non-cattle keeping household. Each cluster contributed two stool samples, two water samples and two soil samples, one of the samples from cattle keeping household and another from a non-cattle keeping household. Isolation, characterization and quantification of the risk of transfer of
Logistic regression was run to quantify risk factors for the presence of isolates from cattle, humans, water or soil which are genetically identical to at least one other isolate from same or different clusters by using PROCGENMOD in SAS as earlier described . The response variable was the occurrence of identical PFGE band pattern of
From 1046 samples, 118 (11.28%) samples produced ampicillin-tetracycline-resistant
Isolates with distinct PFGE band patterns within clusters had a good temporal relationship in terms of sampling and isolation. Most of them came from samples collected on one day or within a week (Table 4) .
|A||6||6B2||6B4||6B6||6H2||16 July 2011|
|7||7B2||7H1||7H2||16 July 2011|
|8||8B1||8H2||8S1||20 July 2011|
|9||9B3||20 July 2011|
|30||30B1||20 July 2011|
|B||36||36B1||21 September 2011|
|38||38H2||21 September 2011|
|D||28||28H2||28S1||15 September 2011|
|4||4B1||15 September 2011|
|3||3S1||22 July 2011|
|E||11||11B1||24 September 2011|
|17||17B2||17S1||15 January 2012|
|18||18S1||15 January 2012|
|40||40W2||15 January 2012|
|20||20B2||20B3||18 January 2012|
|44||44W2||11 January 2012|
|F||33||33H1||20 July 2011|
|9||9S1||20 July 2011|
From univariable analysis, five explanatory variables, namely manure responsible personnel (family member or hired laborer), cattle house roof (present or absent), cattle house floor (concrete or earth), use of bedding (yes or no) and animal water source (tap or surface water) qualified and progressed to multivariable logistic regression analysis. There were no detected confounders during the model building process, and the final logistic regression model was made up of a single explanatory variable, the type of cattle house roof. The cattle house with a roof was at 11 times odds of having isolates with identical PFGE band pattern to another isolate from another source (OR = 11.2, 95% CI 1.1–119.3). Generally, isolates with PFGE band pattern identical to at least one isolate from another source were 33, 86.8% of which were isolated from cattle houses with a roof. The model goodness-of-fit test, expressed as the ratio of deviance to degree of freedom, was 1.2, while the correlation of 0.1344 existed between sample sources from different clusters. This shows that the variables were well explained by the model.
From this study, it seems that there was transmission of bacteria in roofed cattle houses than in cattle houses without roof. This could be due to the effect of direct sun rays in open cattle houses killing the bacteria before the transmission.
Cattle feeding system was statistically associated with cattle water sources (X2 = 28.5, df = 1,
Cattle and manure management practices in urban and peri-urban livestock farming allow direct contact of cattle manure with humans, cattle and the environment. Humans and cattle are at risk of infection with enteric pathogens and the environment to contamination because enteric pathogens have been isolated from fresh cattle feces in urban and peri-urban areas. Under the current manure management system, there is transmission of commensal enteric bacteria between cattle, humans and the environment (water and soil), in which case, same route can transmit enteric pathogens. The risk of human and livestock infection and environment contamination is potentiated by the fact that cattle keepers are unaware of such manure-related pathogens and majority of them do not perceive that there are public health threats from the current cattle and manure management practices. The risk of enteric pathogen transmission to humans extends beyond cattle keeping households to their non-cattle keeping neighbors. Current cattle and manure management practices in urban and peri-urban areas of Morogoro put the whole community (cattle keepers and non-cattle keepers), cattle and other domestic animals, at risk of infection and the environment (water and soil) to contamination.
The reported public health challenges can be alleviated by adopting a system thinking or holistic approach, whereby all stakeholders are identified and involved, at their respective capacities, in planning, execution and monitoring of urban and peri-urban livestock farming. This approach will aim at safeguarding public, livestock and ecosystem health at the same time improving urban and peri-urban livestock contribution toward community livelihood. Some of the key stakeholders, each of whom may have a different key role in ensuring this goal is achieved, include personnel from health section, agriculture, livestock, local government authorities, land use planning, civil engineers, environmental conservation, demography, law enforcing sections, politicians and the general public. For example, local government authorities may put preconditions for starting a cattle herd in urban and peri-urban areas and set criteria for maintenance of livestock keeping permit. This procedure may facilitate other livestock-related activities such as disease control, surveillance and traceability of animals. Moreover, land use planning and environmental conservation sections may set specific areas for keeping livestock, while medical and veterinary sections may jointly control zoonoses. The law enforcing personnel can facilitate in making sure regulations related to livestock, and livestock products are observed. The general public should be well informed of and participate in control of manure-related zoonotic pathogens. The holistic setup of urban and peri-urban livestock farming should take into account all the features of continuous change from rural to peri-urban to urban setting. This means that planning of livestock farming in peri-urban should suit the urban setup even when the peri-urban area is urbanized.
To reduce human and animal contact with manure and to reduce the risk of human and animal infection and environmental contamination, the following strategies are recommended.
Urban and peri-urban land use planning should include livestock industry during planning so that specific areas are legally recognized for livestock farming in urban and peri-urban areas.
There should be strategies to convert manure into a convenient, safe and valuable commodity. This should involve reduction in water content and odor from manure while maintaining its soil fertilizing quality.
Education to community (livestock keepers and non-livestock keepers) on livestock and manure-related zoonotic risks which are associated with management practices. It should be the responsibility of the whole community to ensure one health status is achieved.
Appropriate regulations, by-laws and guidelines should be formulated and reinforced to guide safe cattle and manure management practices which safeguard public, livestock and ecosystem health. The guidelines should clearly give directives on personal protection, cattle and manure handling and environmental protection.
The author wishes to thank the Ministry of Foreign affairs of Denmark through the Danish International Development Agency (Danida) for financial support to the project “Opportunities and challenges in peri-urban livestock farming in Tanzania” (P6-08-Tan), to which this work is a part. The excellent collaboration between Sokoine University Agriculture (Tanzania) and University of Copenhagen (Denmark) during implementation of this study is highly appreciated. Special recognition is granted to Statens Serum Institut (Denmark) for their technical support during laboratory work. I acknowledge participation and project support of the community (cattle keepers and non-cattle keepers) and Livestock Extension Officers in urban and peri-urban areas of Morogoro.