A longitudinal study to identify constraints to dairy cattle health and production in rural smallholder communities in Northern Vietnam

A longitudinal study to identify constraints to dairy cattle health and production in rural smallholder communities in Northern Vietnam

Research in Veterinary Science 81 (2006) 177–184 www.elsevier.com/locate/rvsc A longitudinal study to identify constraints to dairy cattle health and...

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Research in Veterinary Science 81 (2006) 177–184 www.elsevier.com/locate/rvsc

A longitudinal study to identify constraints to dairy cattle health and production in rural smallholder communities in Northern Vietnam K. Suzuki a

a,*

, M. Kanameda b, K. Inui b, T. Ogawa b, V.K. Nguyen b, T.T.S. Dang b, D.U. Pfeiffer a

Epidemiology Division, Department of Veterinary Clinical Sciences, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Herts AL9 7TA, UK b National Institute of Veterinary Research, Truong Chinh, Dong Da, Hanoi, Vietnam Accepted 7 December 2005

Abstract The objective of the study was to investigate constraints to dairy cattle health and production in rural smallholder communities in northern Vietnam, one of the target areas of the Vietnam government’s dairy development programme. A total of 99 dairy farms (11 per commune) were recruited from 9 of 32 communes in Ba Vi District, using random two-stage cluster sampling. After the initial questionnaire interviews were conducted, farms were visited at three monthly intervals over a period of 1 year. Information on several health and production parameters relating to the study cattle was collected. Using multiple indicator modelling, it was found that Fasciola infestation, farmers who had been involved in dairying for longer (not indicative of better management skills), larger herd size, and cattle being kept in a shed were linked to reduced reproductive performances. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Dairy cattle; Longitudinal study; Multiple indicator modelling analysis; Smallholders; Vietnam

1. Introduction The Vietnamese government has developed a policy aimed at the expansion of dairy cattle production in order to satisfy the demand for dairy products in urban areas such as the capital city of Hanoi and alleviate poverty amongst rural farming communities. The policy has directed towards the development of dairy sector through stabilising milk price, supporting the creation of collection centres and marketing channels, and imports of highly productive animals for breeding purposes (Ministry of Agriculture and Rural Development, 2000). Milk production in Vietnam is mainly under the smallholder farmers. There is relatively little published information on most aspects of

dairy health and production including the prevalence of economically important diseases and reproductive performance at the smallholder level in Vietnam. The objective of this paper reporting a longitudinal study is to identify constraints to dairy cattle health and production in smallholder farming communities in which the Vietnamese government’s dairy development programme has been implemented. Particular emphasis was placed on testing the hypothesis that management and health factors influencing dairy cattle reproductive performance could be defined. 2. Materials and methods 2.1. Study area

* Corresponding author. Present address: Rural Development Department, Japan International Cooperation Agency, 2-1-1, Yoyogi, Shibuyaku, Tokyo 151-8558, Japan. Tel.: +81 3 5352 5907; fax: +81 3 5352 5326. E-mail address: [email protected] (K. Suzuki).

0034-5288/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.rvsc.2005.12.002

The Ba Vi district in Ha Tay Province in northern Vietnam was selected (Fig. 1). There were about 500 households involved in dairy cattle farming out of about

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Fig. 1. Map of the nine study communes in Ba Vi District, Ha Tay Province, Vietnam (Delta area; 1–4, Upland area; 5–7, Mountain area; 8 and 9). Dots indicate locations of the 99 study dairy farms.

52,000 households. The total number of dairy cattle was 1100. It is considered typical for the smallholder farming areas adjacent to the capital city of Hanoi (District Veterinary Station in Ba Vi (DVS), 2001, personal communication). Expansion of dairy cattle production has been encouraged by the national government since 1998 in this district. Farmers have been provided a loan for the purchase of dairy cattle, training sessions for new dairy farmers, and free services of artificial insemination and vaccination (haemorrhagic septicaemia and foot-andmouth disease) for their cattle (Ta, 2003). The mean annual temperature in the study area is 21.5 °C. Monthly average rain fall ranges between 40 and 300 mm (Holland et al., 2000). Based on geographical characteristics, all 32 communes of the district are divided into following three groups: Delta (12 communes in the north), Upland (13 communes in the middle) and Mountain area (7 communes in the south). 2.2. Selection of study farms and animals Using random two-stage cluster sampling, 9 of 32 communes in Ba Vi District, where dairy cattle farming had been developed in the district prior to the start of this study, were randomly selected as primary sampling units. As secondary sampling units, a total of 99 dairy farming households (11 per commune) were randomly recruited from the register of the dairy farming households in each commune, provided by the DVS. All dairy cattle owned

by the study households were included. The animals were individually identified for follow-up. Animals were divided into age groups as follows: Calves <1 year old, Heifers P 1 year old and nulliporous/non-porous, and Cows P 1 year old and porous. 2.3. Data collection The longitudinal study consisted of data collection through questionnaire interviews at the beginning and the end of the study period, together with three-monthly follow-up visits. The questionnaires and the production monitoring sheet were prepared by the first author and staff of the National Institute of Veterinary Research (NIVR) in Hanoi. The initial questionnaire interview on farming management practices was conducted by the interview team comprising of the first author, staff from DVS and a commune-based animal health worker. All farms were visited between March 2002 and April 2002. A second questionnaire interview was conducted in March 2003 in order to cross-check the accuracy of the data recorded on the production monitoring sheets by the farmers. In addition, quarter milk samples were examined using the California mastitis test while on farm (Cork and Halliwell, 2002). Follow-up visits were implemented by teams comprising of three animal health workers serving the communes in the selected areas. Prior to the first-visit, these teams were provided adequate practical training by the first author and staff of

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NIVR. Each team visiting a commune spent a maximum duration of three days per follow-up point in time. Cattle body condition scores were measured using a 5-point scale with half-point divisions (Pagot, 1992; Matthewman, 1993). Blood samples were taken from the jugular vein and collected into tubes with and without an EDTA anti-coagulant. Faecal samples were collected from the rectum. 2.4. Laboratory examinations Blood and faecal samples were used for diagnostic investigations at the NIVR. Individual-animal infection status (positive/negative) for selected diseases was the outcome of primary interest. With EDTA blood samples, packed cell volume (PCV) was estimated using a microhaematocrit centrifuge and reader. Plasma total protein (TP) was determined using a clinical refractometer SURJE (Atago Co. Ltd., Japan). Serum samples were tested for antibodies to Mycobacterium bovis, Brucella abortus, Pasteurella multocida, Leptospira interrogans and Theileria spp. using different indirect enzyme-linked immunosorbent assays (ELISA). All tests (except for the ELISA to detect P. multocida) were conducted according to published diagnostic testing standards (OIE, 2000). The diagnosis for P. multocida was based on an ELISA assay developed to measure immunity to Pasteurella in vaccinated animals (Johnson et al., 1988; De Alwis, 1999). Antigen for detection of genus-specific anti-leptospiral IgG in cattle was produced based on 12 serovars of Leptospira interrogans, provided by the National Veterinary Diagnostic Centre in Hanoi, which included all serovars known to occur in the Hanoi region such as australis, autumnalis, bataviae, canicola, grippotyphosa, hebdomadis, icterohaemorrhagiae, javanica, mitis, pomona, saxkoebing and sejore using procedures described by Lottersberger et al. (2002). The identification as well as taxonomic classification of the causative agents of bovine theileriosis occurring in northern Vietnam was still controversial. The serological cross-reactivity between Vietnamese Theileria species and other known Japanese Theileria species was therefore investigated. An ELISA method based on a Japanese strain of T. sergenti as antigen was used (Shimizu et al., 1988). Optical densities (OD) were determined by a Bio-Rad 550 spectrophotometer with 450 nm filter. Cut-offs or upper OD limits of negativity with a 95% confidence limit for each of the tests were determined by staff of the NIVR based on multiplying the standard deviation by 1.96 plus the mean of a known negative sera population for each of the different ELISAs (Crowther, 2001). Faecal samples were processed using standard flotation and sedimentation methods. A sample was classified as infected if at least one endo-parasite ovum was seen using either examination method. Parasites were classified into four classes: trematodes, nematodes, cestodes and protozoa. Species identification was conducted when possible.

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2.5. Data analysis Prevalences were calculated taking into account the random two-stage cluster sampling using the Survey Toolbox version 1.0 (Cameron, 1999). Univariate analyses were conducted for comparison of percentage prevalence of Fasciola spp. in the study dairy cows among the three geographical areas. Exact tests of significance were used when the assumptions of standard asymptotic statistical methods were not met. Confidence intervals of proportions were calculated using Wilson’s method (Dawson and Trapp, 2001). In order to identify factors associated with reproductive performance of cattle, multiple indicator modelling analyses, using the structural equation modelling software EQS 6.1 for Windows (Multivariate software Inc., Encino, CA, USA), were conducted. The 20 observed variables explaining six latent variables involved in this analysis are described in Table 1. The variable CALV_P indicates the proportion of the 130 cows present at the start of the study which calved during the 1-year study period (Hutabarat et al., 1997). The variable HEAT60 represents the proportion of cows recorded as having seen in heat within 60 days after the last calving (Malmo, 1989). The variable 1ST_SR refers to the proportion of conceptions at first artificial insemination during the study period, as diagnosed by commune-based animal health workers through rectal palpation (Radostits, 2001). These three observed variables are used to define the latent variable ‘reproductive performance’. The other 17 observed variables describing the five other latent variables were selected based on published information in conjunction with the prior biological knowledge (Curtis et al., 1985; Erb et al., 1985; Matthewman, 1993; Bonnett and Martin, 1995; Payne and Wilson, 1999; Radostits, 2001; Zwart and Jong, 2001). Variables which can be obtained using relatively objective measurement such as through laboratory examinations, production monitoring records or visual assessment, were prioritised during the selection process. In terms of disease positivity, disease agents which were tested using repeated sampling from the same animals were given priority during variable selection. Univariate analyses were used in order to become more familiar with the relationships among the 17 observed variables for the specified latent variables and the three observed variables for the latent variable ‘reproductive performance’. As the intraclass correlation for variables resulting from random two-stage cluster sampling for the current study were higher than 0.5, two-level structural equation modelling approaches were used (Muthen, 1997). Missing data were imputed using the expectationmaximisation algorithm. Robust maximum likelihood estimation methods were used for modelling of categorical variables with small sample sizes (Bentler, 1995; Bentler and Wu, 1995). The model goodness-of-fit was assessed using indices such as the goodness-of-fit index or GFI and root mean-square error of approximation or RMSEA (Kano and Miura, 2002; Trost et al., 2003).

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Table 1 Latent and observed variables used in the multiple indicator modelling analysis for reproductive performance in the study cows

Table 2 Population dynamics of the study dairy cattle in the smallholder communities during the longitudinal study (March 2002–March 2003)

Latent variable

Age group

Number of cattle at starta

Entries Births

Purchases

Deaths

Sales

Calves Heifers Cows Total

53 (3) 57 130 240

113 – – 113

11 13 1 25

5 1 5 11

61 20 23 104

REPROD: reproductive performance

Observed variable

Observed variable description

CALV_Pa HEAT60a

Calving probability Heat by 60 days after calving First service pregnancy

1ST _SRa CATTLE: cattle profile

HF_Xa

AGE 1ST_CV COND: body condition status

PCV TP CS

POS: positivity for disease agents

LEPTa FASCa STROa THEIa

FARM: farm profile and dairy cattle management practices

TRAINa

EXP_D NUM_C PERM_Sa

WATERa LOSSES: losses from study population

DEATHSa SALESa

a

Holstein Friesian crossbred (0; other breed) Age at the first visit (months old) Age at the first calving (months old) Yearly mean packed cell volume (%) Yearly mean plasma total protein (g/l) Yearly mean body condition score (5-point scale) Positive at least once: Leptospira interrogans Fasciola spp. Strongyle spp. Theileria spp. Participated in at least one dairying training session Years of experience in dairying Number of dairy cattle owned at the first visit Permanent housing in shed (0; grazing during the day) Providing drinking water ad libidum (0; rationed) Deaths during the study period Sales during the study period

Binary variable, coded 1 as Yes and 0 as No.

3. Results 3.1. Description of study population All 99 dairy households from the initial questionnaire interview were included, resulting in a total of 240 dairy cattle at the start of the current study. Table 2 summarises the dairy cattle population dynamics according to age group for the study period. Three households in one of the communes discontinued dairy farming by September 2002 and the other eight households in the same commune refused collection of blood samples from their cattle after the second sampling in September 2002. They expressed concern that their cattle were too weak due to the hot and humid weather. Therefore, data and sample collection

a

Exits

Number of cattle at enda 68 (2) 67 128 263

The figures in parentheses represent the number of males.

were continued only with the cooperating eight communes. Three households in the eight communes discontinued dairy farming during the study period. No samples were taken when farmers expressed concern about the potential impact of sampling on their cattle’s health. Farmers were often reluctant to permit blood and faecal sampling if their cattle were pregnant or had been inseminated shortly before sample collections. This resulted in no samples being taken from 18% of the total number of dairy cattle (n = 251) in June 2002, 38% (n = 231) in September 2002, 44% (n = 256) in December 2002 and 45% (n = 263) in March 2003. A total of 635 blood samples and 538 faecal samples from 239 cattle were included in this analysis. All 99 households were visited during the second questionnaire interview in March 2003. Excluding households that had discontinued dairy farming, all farmers had their cattle vaccinated for haemorrhagic septicaemia once a year (April in the case of the year 2002) and foot-and-mouth disease twice a year. More than 80% used anthelmintic treatments for liver fluke and tick control in their cattle several times a year. Breeding and calving took place throughout the year. All farmers fed colostrum to their newborn calves. Cows were milked by hand twice daily. 3.2. Mastitis test Because of the importance of fresh milk as a source of cash income, farmers were less cooperative with respect to collection of milk compared with blood or faecal samples. Fifty-eight percent of 128 cows were in lactation at the last sample collection in March 2003. For the abovestated reason, 24 cows (32% of the 74 milking cows) were available for the California mastitis test and six (25%, 95% CI 10–47) reacted positive. 3.3. Infectious disease prevalence A small number of samples reacted positive for M. bovis [2% (95% CI 0.4–5, n = 141) in December 2002 and 0.7% (95% CI 0.1–4, n = 142) in March 2003] and B. abortus[0.5% (95% CI 0–3, n = 204) in June 2002 and 0.9% (95% CI 0.1–4, n = 141) in December 2002]. None of the calves had positive results for M. bovis or B. abortus. During the study period, cattle had seroprevalences for P. multocida and L. interrogans of 90% and 25%, respectively.

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Seroprevalence of P. multocida remained low in calves in contrast to heifers and cows. Throughout the study period, the infection prevalence for Theileria parasites was around 15%. Longitudinal serological reaction levels of L. interrogans and Theileria spp. varied considerably in animals. However, the number of serological reactions above the cut-off value increased with the number of repeated samples taken from individual animals (Table 3). When aggregating animals from all age groups that had tested negative during the first sampling and were re-sampled at the three consecutive samplings, the nine-month sero-conversion risk for each disease agent between June 2002 and March 2003 in the current study was as follows: M. bovis: 0% (n = 88); B. abortus: 0% (n = 87); L. interrogans: 9% (95% CI 4–18, n = 67) and Theileria spp. 8% (95% CI 4–17, n = 72). Fasciola spp. [10% (95% CI 5–12, n = 204) in June 2002, 26% (95% CI 19–32, n = 163) in September 2002 and 26% (95% CI 20–33, n = 157) in March 2003] and Strongyle spp. [16% (95% CI 11–20, n = 218) in June 2002, 9% (95% CI 5–14, n = 163) in September 2002 and 11% (95% CI 7–18, n = 156) in March 2003] showed wide variation in prevalence among sampling months (samples not available for testing in December 2002). Prevalence of Fasciola spp. varied between geographical areas and sampling months (Table 4). Other types of gastro-intestinal parasites such as Toxocara spp., Trichuris spp., Moniezia spp. and Coccidia spp. were found in some cattle. Table 3 Percent of sero-positive samples for Leptospira interrogans and Theileria spp. per animal by total number of samples taken per cattle in the study dairy cattle population Number of samples collected per animal

Positive samples per animal 0

1

2

Leptospira interrogans 1 2 3 4

77 70 52 47

23 15 18 25

15 22 16

Theileria spp. 1 2 3 4

84 77 68 61

16 23 18 26

0 10 9

3

8 6

4 3

4

Number of cattle

6

75 26 49 88

1

75 26 49 88

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3.4. Multiple indicator model for reproductive performance Table 5 presents the relationships between the 17 observed variables for the specified latent variables and the three observed variables for the latent variable ‘reproductive performance’. The final model describes the relationship between the independent effects of the cattle profile, disease positivity, farm profile, and population losses and the dependent effect reproductive performance in the study cows (Fig. 2). The goodness of fit information suggests that this model achieved a good fit to the data. Although the factor for body condition status was not significantly associated with reproductive performance, it was not removed from the model because the path coefficients between the factor and its two indicators of nutritional status (TP and CS), which can influence reproduction potential, were significant. 4. Discussion At the start of the current study, the 99 sampled farms represented 20% of all dairy farms in the study area. An appropriate sampling method was used to secure a certain degree of external validity. It must be kept in mind that the refusal of the farmers to have their cattle sampled in blood and/ or milk is likely to be subject to bias in the data collected. Results from the current study provide a description of the risks to dairy cattle health in the study farming systems. None of the animals sero-positive for M. bovis or B. abortus reacted positive on the sub-sequent sampling occasions. Considering the published ELISA specificities of 91% for M. bovis and 90% for B. abortus (Uzal et al., 1995; Lilenbaum et al., 1999) and in the absence of other reported diagnoses from the area, these results were therefore considered to be ‘‘false-positives’’. Immunity to P. multocida in vaccinated dairy cattle had not been measured prior to this study. A high reactivity to P. multocida antigen in ELISA was generally observed in the serum samples collected. The current study describes the spectrum of parasites occurring in dairy cattle in the study area. The observed prevalence of fascioliasis broadly agreed with the prevalence of 22% in cattle in the suburbs of Hanoi reported by Holland et al. (2000). The sensitivity and specificity of the sedimentation method of 67% and 100%, respectively (Anderson et al., 1999). Considering the sensitivity and

Table 4 Prevalence of Fasciola spp. in the study dairy cattle population by geographical region and sampling month Sampling month

Jun 02 Sep 02 Dec 02 Mar 03

Delta area n

% Positive (95% CI)

112 108 n/a 104

5 31a – 25

(2-11) (23-40) – (18-34)

P value (v2 statistic)

Upland area

Mountain area

n

% Positive (95% CI)

n

% Positive (95% CI)

53 25 n/a 33

17a 24 – 27

39 30 n/a 20

0a 3a – 30

(9-29) (12-43) – (15-44)

(0-9) (1-17) – (15-52)

0.004a (11.0, 2 df) 0.009 (9.4, 2 df) – 0.884 (0.25, 2 df)

Values with the same superscript in a row were significantly different based on a multiple comparison between groups using Bonferroni’s correction. n/a: not available for testing. a Exact significance.

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Table 5 Relationships between the indicators for the specified latent variables and the indicators for the latent variable ‘reproductive performance’ for the study cows (n = 130) Variable

CALV_P

HEAT60

Yes (n = 79)

HF_X AGE

TP CS

DEATHS SALES *

Mean (SD)

Median (range)

100

Yes (n = 33) %

Mean (SD)

No (n = 97) %

Mean (SD)

Median (range)

98

Mean (SD)

%

56 (24–126) 27 (20–48) 29.2 (3.0) 72.7 (4.5) 3.7 (7.4)

42 39 12 30

47 29 17 28

91 3 (1–7) 2 (1–8)

Median (range)

99

61 (26–102) 27 (20–30) 29.2 (3.2) 72.9 (4.4) 3.9 (7.4)

85 2* (1–5) 2 (1–8)

No (n = 86) % 98

57 (24–126) 27 (20–48)

52 32 22 32

90 3 (1–7) 2 (1–8)

Yes (n = 44) %

29.3 (3.0) 73.1 (4.6) 3.8 (7.4)

56 44 22 35

89

Median (range)

100

28.9 (3.1) 72.0 (3.7) 3.8 (7.4)

39 18* 16 26

Mean (SD)

62 (26–96) 27 (20–36)

29.5 (2.6) 72.4 (3.4) 3.8 (7.4)

3 (1–5) 2 (1–8)

Median (range)

96 57 (24–126) 27 (20–36)

29.0 (3.3) 73.0 (5.0) 3.7 (7.0)

LEPT FASC STRO THEI TRAIN EXP_D NUM_C PERM_S WATER

No (n = 51) %

60 (26–120) 27 (20–48)

1ST_CV PCV

Median (range)

55 43 23 39

89 2 (1–5) 2 (1–5)

90 3 (1–7) 2 (1–8)

88 35

91 29

89 21

94 37

91 36

89 31

0* 0*

10 51

0 0*

5 27

0 0*

6 30

P < 0.05 (v2 tests for comparison with categorical data and Mann–Whitney U tests with continuous data).

K. Suzuki et al. / Research in Veterinary Science 81 (2006) 177–184

Mean (SD)

1ST _SR

K. Suzuki et al. / Research in Veterinary Science 81 (2006) 177–184

E

HF_X

E

AGE

183

TRAIN

E

EXP_D

E

NUM_C

E

PERM_S

E

WATER

E

CALV_P

E

HEAT60

E

1ST_SR

E

DEATHS

E

SALES

E

1.00 0.40 0.07

CATTLE

0.84 *

- 0.01 E

1ST_CV 1ST_CALV

E

PCV

FARM

0.58 * 0.27 *

0. 17 * 1. 00 E

TP

0. 21*

- 0.24 * C OND

D

0. 21* E

- 0.07

0. 07

CS REPROD

E

0. 42 *

LEPT

0. 51 *

- 0.44 * E

0. 94

0. 41

FASC

- 0.23 *

0. 43 * E

0. 30

POS

STRO

0. 27

1. 00 LOSSES

E

0. 10

THEI

*

P < 0.05. D: disturbance. E: error.

Goodness-of-fit indices: GFI 0.947, RMSEA 0.070. Fig. 2. Final multiple indicator model for reproductive performance in dairy cows for the study smallholder communities in Ba Vi District, Ha Tay Province, Vietnam (standardised solution, n = 130).

specificity above and the results of the diagnostic tests for Fasciola spp. in the current study, each true prevalence of Fasciola spp. in the study population in June, September 2002 and March 2003 was 15% (95% CI 12-17), 39% (95% CI 35–43) and 39% (95% CI 35–43), respectively. A highly variable pattern of sequential serological test results from individual animals for L. interrogans and Theileria spp. infection has been reported (Thiermann and Garrett, 1983; Cousins et al., 1985; Shimizu et al., 1988). These facts can partly explain the results from the current study that suggests substantial variation in individual animals’ ability to react immunologically to Leptospira and Theileria infection (Table 3). The Mountain area is generally considered to have more high land subject to insufficient agricultural water than the other two groups. Such topography may not be suited for the proliferation of the intermediate lymnaeid snail hosts and lower amounts of herbage contamination with metacercariae of Fasciola spp. Low prevalence of Fasciola infection in the study cattle in the MOUNTAIN area in the first and second sampling collection points in time could be explained by the descriptions above (Table 4).

The multiple indicator model was able to demonstrate that Fasciola infestation, long years of experience in dairying, a large number of dairy cattle owned at the first visit, and permanent housing in shed were significantly related to poor reproductive performance of cows. Relationships between Fasciola burden and poor reproductivity and/ or weight losses in cattle are consistently reported in developing countries (Pagot, 1992; Orellana et al., 1999; Holland et al., 2000; Loyacano et al., 2002). Although one would normally expect that farmers improve their management skills with increased experience, in the current study this was not generally the case. The negative effect of an increased number of animals owned can be interpreted as resulting in less individual care for each animal, since the number of household members looking after these animals did not increase. Farmers are likely to underestimate the importance of reducing the adverse or extreme effects of climate for crossbred dairy cattle because of the poor adaptation of these exotic breeds to hot and humid environments. As most of the sheds were fully walled, ventilation was inadequate to remove heat, moisture, micro-organisms and pollutants. Therefore, one practical improvement mea-

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sure would be to let animals graze during the day. Good extension programmes are necessary to inform farmers about appropriate dairy cattle shed designs. Acknowledgments This longitudinal study was carried out as part of the Vietnam-Japan development project ‘Strengthening Capacity of the National Institute of Veterinary Research’ at the National Institute of Veterinary Research, Hanoi, Vietnam. The authors wish to thank in particular all commune-based animal health workers involved and the staff of the District Veterinary Station in Ba Vi for their support. We are extremely grateful to the study farmers who allowed us to work with them during this study. The study was funded in part by the Japan International Cooperation Agency and the ORS Awards Scheme, Universities UK. References Anderson, N., Luong, T.T., Vo, N.G., Bui, K.L., Smooker, P.M., Spithill, T.W., 1999. The sensitivity and specificity of two methods for detecting Fasciola infections in cattle. Veterinary Parasitology 83, 15–24. Bentler, P.M., 1995. EQS Structural Equations Program Manual. Multivariate Software Inc., Encino. Bentler, P.M., Wu, E.J.C., 1995. EQS for Windows User’s Guide. Multivariate Software Inc., Encino. Bonnett, B.N., Martin, S.W., 1995. Path-analysis of peripartum and postpartum events, rectal palpation findings, endometrial biopsy results and reproductive-performance in Holstein-Friesian dairy-cows. Preventive Veterinary Medicine 21, 279–288. Cameron, A.R., 1999. Survey Toolbox – A Practical Manual and Software Package for Active Surveillance of Livestock Diseases in Developing Countries. Australian Centre for International Agricultural Research, Canberra, pp. 1–330. Cork, S.C., Halliwell, R.W., 2002. The Veterinary Laboratory and Field Manual, first ed. Nottingham University Press, Nottingham, pp. 1–497. Cousins, D.V., Robertson, G.M., Hustas, L., 1985. The use of the enzymelinked immunosorbent-assay (elisa) to detect the Igm and Igg antibody-response to Leptospira Interrogans serovars Hardjo, Pomona and Tarassovi in cattle. Veterinary Microbiology 10, 439–450. Crowther, J.R., 2001. The ELISA Guidebook, first ed. Humana Press, Totowa, pp. 1–436. Curtis, C.R., Erb, H.N., Sniffen, C.J., Smith, R.D., Kronfeld, D.S., 1985. Path-analysis of dry period nutrition, postpartum metabolic and reproductive disorders, and mastitis in Holstein cows. Journal of Dairy Science 68, 2347–2360. Dawson, B., Trapp, R.G., 2001. Basic and Clinical Biostatistics, third ed. McGraw-Hill, New York, pp. 1–399. De Alwis, M.C.L., 1999. Haemorrhagic Septicaemia, first ed. Australian Centre for International Agricultural Research, Canberra, pp. 1–141. Erb, H.N., Smith, R.D., Oltenacu, P.A., Guard, C.L., Hillman, R.B., Powers, P.A., Smith, M.C., White, M.E., 1985. Path model of reproductive disorders and performance, milk fever, mastitis, milk-yield, and culling in Holstein cows. Journal of Dairy Science 68, 3337–3349. Holland, W.G., Luong, T.T., Nguyen, L.A., Do, T.T., Vercruysse, J., 2000. The epidemiology of nematode and fluke infections in cattle in the Red River Delta in Vietnam. Veterinary Parasitology 93, 141–147. Hutabarat, T.S.P.N., Pfeiffer, D.U., Morris, R.S., 1997. Factors influencing smallholder cattle production in Indonesia. In: Proceedings of eighth Symposium of the International Society for Veterinary Epidemiology and Economics, Special Issue of Epidemiologie et sante animale 31–32, Paris, 02.13.01-03.

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