Health indicators

Information from routine health management, including coat and body condition as well as physical values such as longevity, growth rate, susceptibility to disease, reproduction and infant care, individual nutritional requirements and wound healing, can be used to assess the welfare of macaques. These are fairly basic measures, however, and will need to be complemented at least by behavioural measures. Indicators of welfare from post mortem examination (e.g. occurrence of enteric pathology), and from regular review of clinical and post mortem records, can also help to identify trends or case clusters that otherwise may not be apparent.

Macaques do not show signs of pain and poor health as obviously as humans; therefore, regular observation and evaluation of health is essential. Keeping detailed records regarding the external condition of individual animals will aid in the early detection of changes indicating poor health. Score sheets (see the tab below) allow records to be kept consistently across time and between staff (who may interpret clinical signs differently). Clinical examinations involving sedation and removal from the group should always be performed by a qualified veterinarian. Click here for mean measurements of anthropometric parameters (e.g. head, waist, total length and weight) for rhesus macaques (scroll to the end of the document).

Changes in health indicators indicative of poor welfare

(Adapted from Tasker 2012; see the tabs above for further information on body condition scoring hair loss, and assessing pain)

Health indicator Changes indicative of impaired welfare
Body condition  Dramatic weight loss such that ribs, hips and spine become visible Body condition scores can differ depending on age, growth pattern and reproductive status.
Dramatic weight gain Condition scoring of weight may be performed non-invasively through observation, or during clinical examination by palpating the thoracic and lumbar vertebrae to assess whether weight changes exceed healthy limits.1
Poor growth Regular condition scoring and body weight assessment at weaning and in the post-weaning period are especially important to ensure young animals receive adequate nutrition to support growth and normal development.2 Monitoring of growth is also especially important for macaques on food and fluid control protocols3 Growth curves are available in the published literature.4
Signs of lameness or imbalance when moving
Wounds May indicate: 1) attack from conspecifics due to problems in social environment (e.g. lack of visual barriers and escape routes for subordinates; or 2) self-harm such as self-biting. Evident wounds indicate advanced pathology, which requires immediate intervention.
Pelage Patchy hair loss Hair loss indicates: 1) an underlying bacterial or parasitic skin infection; 2) self-directed hair plucking due to boredom and stress in an impoverished environment; or 3) hair pulling by conspecifics due to problems in social environment. Novak & Meyer (2009) provide a comprehensive review of possible causes of hair loss.
Reduction in shine and quality
Changes in colour
Faeces Diarrhoea

One of the most common causes morbidity and mortality in captive populations.5 Diarrhoea may indicate acute stress or underlying illness. Carries risk of dehydration, electrolyte imbalance and weight loss.

Post-weaning diarrhoea is predicted by weight at weaning, and also bouts of pre-weaning diarrhoea. These combined factors predict high risk of reduced growth, smaller weight and impaired immune function.6

Urination Excessive urination, lack of urination, or urine drinking
Face Discharge or foam at the mouth, nostrils or eyes
Posture Piloerection or hunched posture Piloerection indicates arousal and may be caused by aggression in the group or towards staff (see the Postures tab under Behaviour). Hunched unresponsive or avoidant posture may indicate pain or depression (see the Signs of poor welfare tab under Behavioural indicators).
Breathing Heavy fast or laboured
Coughing Like humans, macaques catch colds which they recover from naturally. Veterinary assessment is required for coughs, as this may indicate more serious underlying pathology.

 

Body condition can be assessed by visual judgement as to the amount of muscle and subcutaneous fat.7 It can be used as guide to assess level of nutrition8whether the animal is undergoing adequate growth or experiencing poor health (e.g. chronic diarrhoea)9, and as a useful parallel measure with body weight. Two scoring methods for adult rhesus macaques have been published.10 The interpretation of the significance of body condition scores should be made in light of the animal’s current age and reproductive status (e.g. juvenile animals tend to be lean and lanky, scoring as underweight or thin; an animal that has just undergone a growth spurt may be evaluated as thin, whereas one whose growth has stabilized may be lean, as muscle mass catches up with previous bone growth).11 The scoring system however, needs to be sensitive enough to pick up changes in growth and body weight coinciding with events in the laboratory if it is to be a useful welfare assessment tool.

 

Comparison of published body condition scoring methods: rhesus macaques

(Adapted with permission from Clingerman & Summers 2005 and Honess et al. 2005; we recommend reading the full papers)

Clingerman & Summers 2005
Scores awarded based on palpation and visual inspection of whole animal.
Honess et al. 2005
Scores awarded based on palpation of lumbar spine only.
Score Ambulating view Right, back lateral view Score Back view
1 Emaciated 1 0 Emaciated
Hips, facial bones, spinous processes and ribs very prominent. Minimal or no muscle mass over ilium or ischium. Anus recessed between ischial callosities. Body very angular; no subcutaneous fat. No description.
1.5
Very thin
  1.5 1 Severely underweight  Body condition score 1
Hips, spinous processes and ribs prominent. Very little muscle mass over hips and back. Anus may be recessed between ischial callosities. Body angular; no subcutaneous fat. Vertebrae sharp and prominent; distinct gap between each.
2
Thin
 2 2
Underweight
Body condition score 2
Hips, ribs and spinous processes easily palpable. Small muscle mass over hips and lumbar region. Minimal subcutaneous fat. Vertebrae smooth and prominent; gap detectable between each.
2.5
Lean

 

2.5

Hips and spine feel firm. Hips and spinous processes readily palpable; not prominent. Body less angular. Thin layer of subcutaneous fat.
3
Optimum
3. 3
Normal
Body condition score 3
Hips, ribs and spinous processes palpable; not visible. Well-developed muscle mass and subcutaneous fat layer. No abdominal, axillary or inguinal fat pads. Vertebrae smooth and round, and slightly prominent.
3.5 Slightly overweight  3.5
Hip bones and spinous processes palpable with firm pressure but are not visible. Bony prominences smooth. Rib contours are smooth and only palpable with firm pressure. Small abdominal far pad may be present.
4
Heavy
 4 4
Overweight
Body condition score 4
Hips, spinous processes and difficult to palpate. Body contours smooth, less defined. Fat deposits accumulating in axillary, inguinal or abdominal areas. Vertebrae just detectable with pressure.
4.5
Obese
 4.5
Hips and spinous processes difficult to palpate. Bony contours smooth and poorly defined. Prominent fat pads in inguinal, axillary or abdominal region. Abdomen pendulous.
5
Grossly overweight
 5  5
Obese
Body condition score 5
Hips, ribs and spinous processes palpable with deep pressure. Large fat pads in inguinal, axillary and abdominal regions. Pronounced fat deposits. Vertebrae not detectable.

 

Condition scoring by palpation

Body condition can also be scored by palpating the monkey over its thoracic and lumbar vertebrae (at the level of the last rib), making a judgement as to the amount of fat and muscle covering the bony prominences of the vertebrae and giving a quantitative score.

(Adapted with permission from Wolfensohn & Honess 2005)

Vertebrae

Hair loss can be common amongst captive primates, but is not so prevalent in wild animals12, suggesting that some aspect of the captive environment contributes to abnormal patterns of loss.13 It has a complex aetiology and is a multifactorial problem with many contributing factors14. Poor health, such as parasitic infections and skin diseases15, nutrient specific deficient diets16, hair pulling or over-grooming17, stereotypical trichotillomania due to boredom and/or social stress18 and reproductive conditions19 have all been attributed as reasons for hair loss. The seasonal “molt” shown by rhesus macaques on Cayo Santiago is considered by some to be a natural, reversible phenomenon associated with reproductive seasonality.20

Treatment via various behavioural methods (e.g. additional environmental enrichment)21 does not always succeed in producing a reversal in severity22, and therefore the link between hair loss and reduced welfare may be an oversimplification. Nonetheless, given its prevalence in captive animals, particularly in environments (social and physical) considered to be challenging to welfare, and that recipients of hair pulling often show fear or avoidance reactions23 which are likely to reflect poor welfare24, quantifying alopecia may be a useful tool for welfare assessment. Scoring involves estimating the severity and extent of hair loss according to a five point scoring system.25

 

Method for alopecia scoring: rhesus macaques

Adapted with permission from Honess et al. 2005. We recommend reading the full paper.

Score Description Back view
1 Good coat condition; complete cover Alopecia a1 Alopecia score 1b
2 Small patches of alopecia (2-5cm2)  Alopecia score2a  Alopecia score 2b
3 Large patches of alopecia (5cm2)  Alopecia score 3a  Alopecia score 3b
4 Generalised alopecia (>50% of the back)  Alopecia score 4a  Alopecia score 4b
5 Back completely bald; more skin visible than hair  Alopecia score 5a  Alopecia score 5b

Traditional methods of pain recognition and assessment in macaques rely on gross behaviour. Signs of pain may include:26

  • sitting in a huddled position, or crouched with head forwards and down with arms across the body
  • sad expression with glassy eyes
  • reduced movement
  • reduced appetite and/or reduced interest in food treats
  • lack of grooming or poor coat
  • avoiding conspecifics and/or staff
  • increased attention from cage mates
  • facial contortions, clenching of teeth
  • restlessness and shaking, accompanied by vocalisation (e.g. grunts, groans)
  • touching, pushing or scratching the painful area; self mutilation
  • increased or decreased aggressive toward caregivers (or other change in normal behaviour)

Behavioural signs such as these may not be specific to pain, and there is a need for more objective, rapid and reliable measures so that pain can be identified and alleviated more effectively. Researchers funded by the NC3Rs are validating the use of facial expressions for post-operative pain assessment in rhesus macaques, using a research tool established for analysing facial movement – the Macaque Facial Action Coding System. A grimace scale has been developed, similar to those for the mouse, rat and rabbit.

Pain tolerance varies between individual macaques, so each animal should be individually monitored with respect to the need to administer analgesics.

DCF 1.0Quantitative assessment of well-being can be usefully recorded with clinical or welfare assessment score sheets. Their use removes the variation in interpretation of clinical and behavioural signs that is sometimes found between care staff and researchers. Ideally score sheets should be tailored to the specific condition or experiment staff are dealing with.27 Some examples are given below.

In the case of numerical score sheets, a number of clinical signs, physical indicators and behavioural parameters are assessed and given a score according to their apparent severity. Often scores are added up and the results used to determine whether action is needed (such as analgesia) according to a predetermined key attached to the sheet. The animal is reassessed at appropriate intervals to monitor its progress and response to any treatments.

See Hawkins et al. 2011 for general advice on defining and implementing score sheets.

 

Examples of welfare assessment score sheets

1. Objective measures of health and well-being in laboratory rhesus monkeys (Macaca mulatta)

Smith et al. (2006) have developed and validated an objective and quantitative system for assessing and monitoring the health and well-being of laboratory rhesus macaques; specifically those used in long-term neurophysiology studies with fluid control. Observations are made twice a day by an experienced observer and checklists used to record: (a) potentially life-threatening clinical concerns; (b) developing clinical issues; (c) atypical behaviours; and (d) laboratory performance. The authors demonstrate with two case studies the utility of their multidimensional system for identifying incipient clinical and behaviour problems before they become serious. Although observations were made twice daily, the authors comment that a single daily measure would be sufficient.

2. Handbook of primate husbandry and welfare

Wolfensohn & Honess 2005 present an example sheet for monitoring a monkey with a neurological deficit (p.62-63).


 

General welfare assessment score sheet

(Adapted from Wolfensohn & Honess 2005)

The welfare assessment score sheet below is presented to illustrate the general principles. It should be modified to provide specific information on the condition or research model under investigation.

 

PARAMETER ANIMAL ID:  SCORE DATE/TIME DATE/TIME
Appearance Normal 0
General lack of grooming 1
Coat staring, ocular and nasal discharge 2
Piloerection, hunched up 3
Food and water intake  Normal 0
Uncertain: body weight decrease of <5% 1
Intake: body weight decrease of 10-15% 2
No food or water intake 3
 Clinical signs  Normal temperature, cardiac and respiratory rates 0
Slight changes in the above 1
T ± 10°C, C/R rate change of 30% 2
T ± 20°C, C/R rate change of 30% or large decrease 3
 Natural behaviour  Normal 0
Minor changes 1
Less mobile and alert, isolated from companions 2
Vocalisation, self-mutilation, restless or still 3
 Provoked behaviour Normal 0
Minor depression or exaggerated response 1
Moderate change in expected behaviour 2
Reacts violently, or very weak and precomatose 3
SCORE If you have scored a ‘3’ more than once, score an extra point for each ‘3’ 2-5
TOTAL 0-20
JUDGEMENT  0-4 Normal
5-9 Monitor carefully, consider analgesics/other treatments
 10-14 Suffering, provide relief, observe regularly
 15-20 Severe distress, consider euthanasia

After any veterinary or research procedure, monkeys should be monitored for signs of adverse effects. Health indicators may be also used to be measure an animal’s adjustment to scientific protocols over time.

Monitoring vaccinated monkeys from NC3Rs on Vimeo. In this video, the member of staff is able to assess all animals from close quarters, including inspecting their physical state, social interactions, appetite for food, movement, presence of diarrhoea, and evidence of pain or aggression. (Video: Wolfensohn & Finnemore 2006)

 

Inspecting head implant from NC3Rs on Vimeo. In this video, a rhesus macaque trained to accept treats from the hand and to permit touching of its body, comes forward to the front of the enclosure, where the head implant used for MRI studies can be inspected for signs of infection without the need for capture or restraint.

 

Hand inspection from NC3Rs on Vimeo. The cynomolgus macaque in this video has been trained to offer its hand for inspection of its digits, as part of routine health monitoring.


  1. Clingerman & Summers 2005; Wolfensohn & Honess 2005 

  2. Wolfensohn & Honess 2005 

  3. Prescott et al. 2010 

  4. van Wagenen & Catchpole 1956; Turnquist & Kessler 1989; Schapiro & Kessell 1993Ribeiro Andrade et al. 2004Vancata et al. 2000Prescott et al. 2010 

  5. Wilk et al. 2008; Prongay et al. 2013; Kanthaswamy et al. 2014 

  6. Wolfensohn & Honess 2005 

  7. Clingerman & Summers 2005; Wolfensohn & Honess 2005 

  8. Clingerman & Summers 2005 

  9. Clingerman & Summers 2005 

  10. Clingerman & Summers 2005; Honess et al. 2005 

  11. Clingerman & Summers 2005 

  12. Honess et al. 2005; Zhang 2011 

  13. Beisner & Isbell 2009 

  14. Beisner & Isbell 2009; Novak & Meyer 2009 

  15. Steinmetz et al. 2005 

  16. Isbell 1995 

  17. Reinhardt et al. 1986; Reinhardt 2005 

  18. Steinmetz et al. 2006 

  19. Davis & Suomi 2006 

  20. Vessey & Morrison 1970; Kessler 2009 

  21. Novak & Meyer 2009 

  22. Kramer et al. 2010 

  23. Reinhardt et al. 1986 

  24. Honess et al. 2005 

  25. Honess et al. 2005 

  26. Wolfensohn & Honess 2005; International Primatological Society 2007 

  27. Wolfensohn & Honess 2005 

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