Scorecard method for assessing the severity of peste des petits ruminants in sheep and goats

Abstract

A methodology to assess the clinical severity of peste des petits ruminants (PPR) in sheep and goats in the field condition was developed using a scorecard by considering five specific cardinal clinical signs (pyrexia, oculo-nasal discharge, oral lesions, respiratory signs, and diarrhoea) of disease. The scores were assigned for the signs based on the severity of the disease that ranged from 1 (low) to 4 (high). The assigned weightage for signs, morbidity, and mortality was 0.75, 0.05 and 0.2, respectively summing up to unity. The scoring and weightages and guidelines were devised by Delphi technique based on the field investigation, field veterinarian’s assessment and specific inputs from PPR experts. The estimated Weighted Score Index (WSI) was considered to classify the severity into mild (WSI < 40) or moderate (WSI 41–60) or severe (WSI > 60) form. This scorecard will help preliminarily to the extent for the identification of the suspected flocks with a required case definition at the first instance, before making decisions on what merits further field investigation. This is first of its kind of methodology to assess the disease pattern in small ruminants and could be used as a disease severity assessment tool in different geographical areas in endemic settings.

Peste des petits ruminants (PPR) otherwise known as “plague of small ruminants”, is a highly infectious and transboundary animal viral disease of domestic and wildlife small ruminants and is caused by small ruminant morbillivirus (SRMV) (http://ictvonline.org/virusTaxonomy.asp). The disease is associated with high morbidity and mortality in susceptible sheep and goats and poses a heavy threat to the national economy of the enzootic countries [1]. The disease with clinical manifestation of high fever, discharges from the eye and nasal orifices, oral ulcer with stomatitis, and enteritis was first reported in 1942 in Côte d’Ivoire, West Africa, since then the PPR has spread to different regions of the world [1, 4]. Considering the importance of small ruminants in food security, socio-economic growth and the disease impact of economic loss of USD 1.45–2.1 billion annually, Food and Agricultural Organization (FAO) and the World Organization for Animal Health (OIE) launched a global plan to control and eradicate PPR by 2030 [13]. Generally, PPRV Infection produces a wide spectrum of clinical manifestations in sheep and goats, with varying severity ranging from mild and short-lived to lethal forms during the course of infection, depending on various factors, like, strain of virus, sensitivity of the host species, breed, age and immune status of animals or individual animal susceptibility [3, 6]. PPR may have an acute and severe course and exhibit different clinical signs in affected animals [11, 18]. In literature, the difficulty of reproducing observed PPR clinical signs in the field condition under experimental situations had been proved [6]. The reasons for this are currently unknown; however, it could be due to a reduced susceptibility or genetic resistance of the sheep or goat breeds used in the studies or reduced virulence of the infecting virus, due to storage or cell passage of the virus in the laboratory [6]. Nevertheless, these researchers, developed experimental challenge protocol for clinical scoring, using a tissue culture passaged virus, which reliably and consistently produced clinical signs of PPR and can be used for quality-controlled vaccine efficacy as well as for pathogenesis studies under experimental conditions. This scoring approach enabled the precise monitoring of the progress and distribution of virus throughout the experimental infection [14].

PPR vaccination produces immune population in particular geographical regions over a period of time through mass vaccination strategies [4] and also financially viable [10]. The vaccine is effective in the face of natural outbreaks and significantly reduce the mortality pattern in the target vaccinated population. The vaccination strategies adopted in any country or region or geographical location will alter PPR epidemiology in general and disease severity pattern in particular, as changing pattern in term of the severity of gross lesions and clinical signs observed in the region, where vaccination was regularly carried out [2, 8]. Further, the disease conditions may not always produce all the clinical signs of PPR but may produce one or more of the classical clinical signs. Notably, the observed mild form of rinderpest (RP) in the last phase of eradication caused delay to declare the eradication of RP [7]. India has practiced focus vaccination in outbreak places since 2002 [17] and progressive and mass vaccination under program mode in some endemic states of India since 2011 [4] even before the global network plan was developed to control and eradication of PPR [13].

Therefore, it is imperative to study the occurrence and its severity patterns in field condition in different regions, which would be helpful in proposing strategic formulation for effective disease management. In this scenario, a methodology is highly imperative to assess disease severity pattern as well as to compare the clinical manifestation in unvaccinated and vaccinated areas or regions, where the changing pattern in term of the severity of gross lesions and clinical signs occurs [8]. As of now, there is no such tool or methods available for assessing the disease severity in sheep and goats in the field condition. Therefore, a scorecard methodology has been developed using the disease-specific inputs and rational assumptions from field investigation of outbreaks.

The clinical scorecard was developed using the Delphi technique [12, 19] comprising national and international experts working in different laboratories on PPR. Besides researchers, the opinion of the field veterinarians was also considered in the developmental stage to include real-life outbreak situations typically observed by veterinarians in the enzootic country, like India. The components of the scorecard were designed based on the literature survey [1, 14] and using certain disease-specific inputs acquired during field investigation of outbreaks by authors and rational assumptions. The national and international expert panel of researchers were finalized and the opinions were invited, collated and summarized for the preliminary scorecard. During round one, the experts were asked to comment on the clinical signs, scoring pattern, weights assigned, a number of samples to be surveyed, severity pattern, etc. During round two, the refined scorecard was again circulated to the experts through email and opinions were received. Thus, the final scorecard was field evaluated during the outbreak’s investigation as well as independent assessment through the field veterinarians.

The number of animals to be selected for scoring was 10% of PPR affected animals (5% each young and adult) based on the incidence or incremental prevalence ranges of 5–10% [4, 9]. The affected animals were selected randomly from either sheep or goats or mixed flock as the case may be and scores were assigned for individual animals. While scoring the affected animals, formulated guidelines (Table 1) were followed for assigning scores that ranged from 1 (low) to 4 (high), based on the clinical severity of PPR. The assigned total weightage for PPR specific clinical signs, morbidity and mortality was 0.75, 0.05 and 0.2, respectively, summing up to unity (Table 2). The classic clinical signs are highly correlated to a different stage of PPRV infection in the field condition at different outbreaks areas. As the survey in PPR affected flocks will be undertaken at different point of time and various stages of infection, it is assumed that, all possible severity levels will be accounted while scoring the disease pattern in the filed condition. Hence, it is assumed that scoring in different outbreaks places and stages of infection can capture the variation in the severity levels of the disease. Further, the estimated Weighted Score Index (WSI) was calculated to classify the severity of outbreak in sheep and goats into mild (if WSI is < 40) or moderate (WSI 41–60) or severe (WSI > 60) form.

Table 3.

Weightage score system to be considered for different morbidity and mortality levels in the PPR infected sheep and goats’ flocks

Score	Morbiditya (%)	Mortalityb (young mortality) (%)	Mortalityc (adult mortality) (%)
4	> 76	> 31	> 15
3	51–75	21–30	11–15
2	26–50	11–20	6–10
1	1–25	1–10	1–5
0	< 1	< 1	< 1

^aMorbidity % in the flock

^bMortality % in the flock for animals < 1-year age

^cMortality % in the flock for animals > 1-year age

Table 1.

Scoring pattern for assigning appropriate score for clinical signs in affected individual sheep or goat

PPR specific clinical signs	Clinical score sheet assessment of animals
	0	1	2	3	4
Signs	Apparently healthy animals	Mild infected animals	Inactive and depressed with inappetance	Inactive, apathetic, restless and anorexic	Severe depression, unable to stand, extreme lethargy, dehydration
Temperature in Fahrenheit (°C)/Pyrexia	< 103 °F (< 39.4 °C)	103–103.9 °F (39.4–39.9 °C)	104°–104.9 °F (40–40.4 °C)	105°–105.9 °F (40.5–41.0 °C)	≥ 106 °F (≥ 41.1 °C)
Nasal/ocular discharges	No discharge	Watery ocular discharge (serous type)	Watery to mucoid oculonasal discharge with congestion of mucosa in the eye (reddened eye with mild conjunctivitis)	Mucopurulent discharge from nostrils and/or eyes and/or with severe conjunctivitis	Profuse mucopurulent discharge with some time crust formation in nostrils and eyes
Oral lesions/mucosal lesions	No visible lesion on the mucous membrane	Reddening of the oral mucous membrane or ulcers (congested oronasal mucosa and buccal papillae)	Few necrotic spots-pin-prick lesions with buccal cavity, sometime more extensive. Ulcers (diphtheritic plaques) -bran like deposit-on mucous membrane, tongue, dental pad, hard palate, cheek	Clear erosive lesions on oral mucosae; severe congestion, oedematous buccal papillae nasal Peel off of mucosa with haemorrhages in oral	Severe erosive lesions throughout buccal cavity, oedematous lips, or dried lesions on oral commissure, etc.
Respiratory sign/cough	No respiratory signs/cough (normal rate 15–40/min)	Very mild cough with bronchitis or rales (slight tachypnoea)	Moist and productive cough (tachypnoea and mild cough)	cough with abdominal breathing (tachypnoea and dyspnoea with presence of coughing)	Severe cough with peculiar pneumonic symptoms (marked tachypnoea/dyspnoea/cough)
Diarrhoea	No diarrhoeic symptoms (normal)	Mild diarrhoea (soft)	Watery diarrhoea (runny)	Severe diarrhoea with soiled hind quarters (frank diarrhoea)	Severe with soiled hind quarters plus blood mixed type (muco-haemorrhagic diarrhoea)

Table 2.

Scoring pattern, weightage, calculation of index for assessing severity pattern of PPR in sheep and goat flock

A. Clinical sign	Animal No. 1	Animals No. 2	Animals No. 3	Animals No. 4	Animals No. 5	Average score (A) total score/no. of animalsa	Weightage-(B)	Weighted score (A × B)
Temperature/pyrexia	Score to be assigned appropriately for clinical signs in affected individual animal by referring guidelines in Table 1						0.15
Nasal/ocular discharges							0.20
Oral lesions							0.10
Respiratory sign/cough							0.15
Diarrhoea							0.15
B. Morbidity %	Scoring based on the morbidity % in the flock					b	0.05
C. Mortality %	Scoring based on the Young mortality % in the flock					c	0.08
	Scoring based on the Adult mortality % in the flock					d	0.12
						Total		Weighted score (WS)

Scoring pattern of five infected animals in the sheep and goat flock size of 50

^aMinimum five animals to be surveyed in a flock of 50 animals

^bMorbidity % in the flock

^cMortality % in the flock (for animals < 1-year age)

^dMortality % in the flock (for animals > 1-year age)-^{b, c, d} Score to be filled directly by referring the Weightage score system (Table 3) for morbidity and mortality

Weighted Score Index (WSI) = Total Weighted Score (WS) × 100/4. If WSI is < 40-mild form or WSI 41–60-moderate or WSI > 60-severe form of disease in sheep and goats flock

The developed scorecard was evaluated by the field veterinarian/or by our scientific team during outbreaks in a few geographical locations to assess the disease severity pattern in sheep and goats flocks. During the investigation, the basic information of the flock, epidemiological data, clinical samples for confirmative diagnosis was also collected. The collected ante- and post-mortem clinical or tissues samples were stored at − 80 °C and were tested for PPRV antibodies, antigen and genomic nucleic acid by serological [15, 16] and molecular assays [5] to confirm the outbreak as PPR.

On analysis of the scoring pattern and weightage assigned during the preliminary stage, the average weightage derived was 13.11%, 14.58%, 14.50%, 19.84%, 19.42%, 9.56%, 10.44%, for pyrexia, discharges, oral lesions, respiratory signs, diarrhoea, mortality, and morbidity, respectively. Further, based on the experts’ comments, the refined weightage for above clinical signs was 15%, 20%, 10%, 15%,15%, 20% (adult 12% and young 8%), and 5%, respectively. The established clinical scoring system with weightage and devised index for observed clinical disease in the field condition is equivalent to the described score system of 0–3 for experimental infection [14]. On-field evaluation of the scorecard by the authors revealed (data not shown) that out of 11 confirmed outbreaks in the region, eight outbreaks involved with the moderate form (WSI ranged from 46 to 59.3), two in the severe form (WSI 69.5–71.8) and one in mild nature (WSI 35.8). These outbreaks were confirmed as PPR based on the positive results of clinical samples by PPR ELISA and PCR assays. Further, the mild or moderate form of the disease was observed in earlier vaccinated areas of the villages, whereas the severe form occurred in the places where the vaccination was not practiced continuously in the preceding 3 years.

Further independent assessment of disease pattern during 28 outbreaks investigation by the field veterinarians in different geographical areas (data not shown), showed that, five outbreaks involved with the moderate form (WSI 42.5–52.5) and two with severe form (WSI 67.5–77.4) and rest of the 21 outbreaks with mild forms (WSI 20–40). In overall, these indicate the occurrence of a mild form in the vaccinated regions, which was concurrent with the earlier observed report by Gomes [8], the changing pattern of disease with the mild lesion and exhibiting milder indicators of clinical signs in the vaccination program implemented region. Moreover, the severity of disease can often vary from outbreak to outbreak regarding the species affected, more severely (sheep vs. goats), the ages affected and the extent of morbidity and mortality, as well as clinical severity would vary in a geographic area based on the extent of vaccination coverage [2, 8].

If developing enzootic countries are implementing national PPR control and eradication program in support of the FAO and OIE Global Eradication Campaign, then at the eradication stage requires a program of syndromic surveillance to identify all potential cases of possible PPR. The mild and occult forms of RP observed in cattle [7], in the last phase of Global Rinderpest Eradication Programme (GREP) surveillance, hindered the recognition of the disease in the eradication phase of RP. Similar situation may arise during the end phase of the PPR eradication stage, where it will be difficult to recognize the mild form in sheep and goats. This is important especially in the face of the appearance of new lineages of PPR virus, which often present with mild clinical signs that vary quite significantly from the established ones. In this situation, the scorecard will help preliminarily to the extent for the identification of the suspected flocks or cases, with a required case definition as well as a combination of the cardinal signs, at the first instance, before making decisions on what merits further field investigation for the suspected cases identification and diagnosis as PPR by reliable confirmative penside or laboratory assay/test and final stamping out decision.

In conclusion, the developed PPR clinical scorecard is first of its kind on methodology to assess the clinical disease pattern of PPR in sheep and goats in the field condition and could be used as a disease severity assessment tool in different geographical locations in endemic settings. However, further validation to be done in wider geographical settings in different agro-climatic zones and time frames, for making it as a suitable methodological tool.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.