Active and passive: Style and use

In some genres of writing – science reports, for example – the passive voice is encouraged. However, many advocates of ‘plain English’ argue that the passive voice can be confusing to readers, and obscures meaning.

The examples below are from articles on the natural sciences, taken from the ICE-GB corpus. They illustrate the use of the passive voice (verb phrases in the passive are highlighted):

  • This process is known as ‘sloughing-off’ and the detached film is collected in a humus tank. [W2A-021 #28]
  • Consequently, these monomers may be metabolised in the absence of oxygen. [W2A-021 #48]
  • A point will be reached where the thickness of the film prevents sufficient nutrients reaching the layer of microorganisms. [W2A-021 #26]

Perhaps because the word ‘voice’ also has broader meanings in English, the passive voice often causes confusion to some people. Take a look at the following examples from the blog Language Log which have all been identified (wrongly) as passives:

  • we have decided ...
  • we will be implementing a program
  • the misfortune that befell Germany and Europe
  • the Reich had to face a superior coalition
  • the war turned out to be ...
  • It was above all the bloody reckoning

None of these are actually passives. If you look carefully at the verb phrases, you will see that none of them have the auxiliary verb be followed by a past participle.

In the transcript below, the passive verb phrases are marked. Click on the '+' symbol to expand the extract.

Note: You might notice that some of them have an -ed participle verb but no auxiliary be – these are special nonfinite passive clauses. They can be expanded into full finite passive clauses with be. Take the example ‘the term “flux”, as used here’. This could be expanded to ‘as it is used here’.

Reduction in the amount of ATP used

In metabolic terms this means reduction in fluxes that utilize ATP.The term ‘flux’, as used here, means the rate of flow of material through a chemical pathway, or the rate of transfer from one site to another, with units amount / time.Since ATP is used up in muscular contraction, a reduction in muscular work, as discussed above, would be one way of reducing total ATP flux.We must now consider the very large component of energy expenditure that is not involved in physical work, namely the basal or resting metabolic rate.The BMR does, of course, include the cost of some muscular work, such as that needed for respiration and circulation of the blood.

Values for the BMR collected from all over the world show that in tropical countries the rate per kilogram body weight tends to be some ten per cent lower than in Europe or North America (Schofield et al., 1985; Henry & Rees, 1988).It is not absolutely clear how far, if at all, this is a climatic effect.Mason, an American missionary, found that her BMR fell every time she moved from Boston to India (Mason & Jacob, 1972), and Sir Charles Martin, who recorded his BMR every day during a 35 day voyage to Australia, found a distinct fall when his ship entered the Indian Ocean and a rise to the original level when she reached the south-easterly Trades (Martin, 1930).On the other hand, Eijkman (1924) stated that his BMR was the same in Batavia (Dutch East Indies) as in Holland.

Shetty (1984), working in Bangalore, India, found that labourers with a very low BMI (average 17.6) and a low energy intake (average 1600 kcal per day), had BMRs per kg that were about 10 per cent lower than those of well-nourished controls in the same environment and 17 per cent lower than the rates expected from the prediction equations of Schofield et al. (1985).McNeill et al. (1987), in studies on peasant farmers in Tamil Nadu (South India), with an average BMI of 19, also found BMRs lower than the predicted rates.They attributed this to differences in body weight and body composition, rather than to a true reduction in the metabolic rate of the tissues.The difficulty with this explanation is that people with a low BMI would have less body fat; moreover, judging by the experimental evidence, any reduction of lean body mass is likely to be mainly at the expense of slowly metabolizing tissues, particularly muscle.One would therefore expect small lean people to have higher BMRs per kilogram than their heavier and fatter Western counterparts.

These studies were on people who had probably been exposed to low energy intakes throughout their lives.The classical experiment of Keys and coworkers (1950) on semistarvation in North American volunteers is, however, relevant because it was continued for six months.James & Shetty (1982), reanalysing the results of that experiment, concluded that ‘the small (sic) fall in BMR per unit active tissue mass (by 16 per cent) in the first 2 weeks remains essentially unchanged for the subsequent 22 weeks of semistarvation’.A 16 per cent fall is, however, not so small, particularly when one takes account of the probable preferential loss of muscle.Therefore it is logical to look at two of the main components of BMR, protein turnover and ion-pumping, to see how far they might contribute to such a reduction.

Protein turnover

As I said at the beginning of this paper, where there is no variability there is no capacity for adaptation.It is therefore relevant that quite a large range of variation has been observed, perhaps two-fold, in the rates of protein turnover of different individuals (Waterlow, 1988).We do not know the advantages or handicaps of having a high or low rate of whole body protein turnover, nor do we know the effects on it of a habitually low energy intake.We are currently engaged in measuring these rates in Professor Shetty ’s subjects.It is generally accepted that protein turnover may account for 15 - 20 per cent of the BMR (Waterlow, 1986), although Jackson (1985) suggested that it may be more.A reduction of one quarter, which is well within the observed range of inter-individual variation, could thus produce a saving of five per cent of the BMR.It should be noted also that the rate of protein turnover is influenced by the activity of the thyroid gland.This has been shown for whole body turnover in obese patients treated with triiodothyronine (Nair et al., 1981; Wolman et al., 1985), and for muscle protein turnover in the rat (Jepson, Bates & Millward, 1988).


The concentrations of sodium, potassium and calcium inside and outside cells are very different, and it takes energy to maintain these concentration gradients.What are colloquially called ‘pumps’ keep sodium out and potassium in.We know the energy cost of pumping one mole, but it is unknown how much energy is used for this process per unit time in the body as a whole.Early estimates (Edelman, 1974) put the cost of Na + - K + pumping at 20 - 45 per cent of BMR.More recent studies (Biron et al., 1979) suggest a much lower figure a maximum of 12 per cent.The concentration of free calcium inside cells is lower than outside by about two orders of magnitude, and it is of crucial importance for many vital processes that the internal concentration should be maintained at the correct level.The cost of calcium pumping may be substantial, but I know of no values for the whole body.

As in the case of protein turnover, Na + - K + pumping is affected by thyroid hormones.Apparently they do not alter the efficiency of the pumps, but their number (Biron et al., 1979; Kjeldsen et al., 1984); in other words, they produce changes in flux rate.Here again, the capacity to vary provides opportunities for adaptation.

Futile cycles

There are a number of metabolic reactions which go backwards and forwards, producing no net chemical work but only heat.It has been calculated that six of these reactions that have been fairly well characterized might normally account for 1-15 per cent of the BMR (Reeds, Fuller & Nicholson, 1985).There is evidence in at least one case of the activity being greatly reduced when an animal is starved (Challiss, Arch & Newsholme, 1985).It has been suggested that these cycles, which appear simply to waste energy, have in fact a regulatory function (Newsholme, Challiss & Crabtree, 1984).If so, reducing the waste of energy as an adaptation to starvation would be at the cost of losing some of the capacity for fine control.

Efficiency of ATP production

The amount of ATP produced per unit of food energy used or of oxygen consumed varies a little with the nature of the foodstuff oxidized and the route of oxidation.Elia & Livesey (1988) give a very comprehensive and up-to-date review.A typical Third World diet, being low in fat and protein, would be about three per cent more economical than a Western diet.The difference is not large, but every little helps.The difference will be increased if, on the Western diet, some of the carbohydrate is cycled through fat before being oxidized.This process involves an energy loss of some 20 per cent (Milligan, 1971).

These calculations are based on conventional values obtained in vitro for the P: O ratio (moles ATP formed per mole oxygen used).In recent years it has become apparent that this process may not always be maximally efficient and that there may be some degree of ‘uncoupling’ of oxygen utilization and ATP formation.The result would be a greater loss of oxidative energy as heat.The extreme example of uncoupling is shown by brown adipose tissue, which produces heat without any formation of ATP.This tissue probably does not have any important function in adult human subjects.However, the basis exists for speculating that in some people oxidation might be more tightly coupled than in others, so that food energy would be used more efficiently.Stücki (1980), in experiments in vitro, has shown that maximum rate and maximum efficiency are incompatible.He uses the analogy of a car: to cover a distance at the least cost of fuel you do not drive as fast as you can.We reach exactly the same conclusion as in our consideration of the energy cost of walking (Fig. 2.1).

Efficiency of ATP utilization

For the reactions considered so far the relationship between the amount of ATP used and the amount of chemical work done is probably fixed.Thus it is thought to take one mole of ATP to pump out three moles of sodium ions, two being exchanged for potassium, and four moles to bind together two moles of amino acids in the synthesis of protein.Even though we may not know the numbers exactly, they are fixed by the nature of the chemical reactions.To return to our analogy: there is probably no way of getting better value for the money spent.

However, muscular contraction provides an exception that is related to mechanical rather than chemical work.The energy that makes the components of a muscle fibre slide along each other when the muscle exerts a pull is ultimately derived from the breakdown of ATP.The relation between the force developed or the amount of mechanical work done to the amount of ATP used is called the contraction coupling efficiency.It has long been known that muscle fibres can be divided into two principal types: the slow-twitch (ST), oxidative or red fibres and the fast-twitch (FT) glycolytic or white fibres, with some intermediate types (see Saltin & Gollnick, 1983).Some muscles are functionally slow and have a predominance of ST fibres; others are fast and contain mainly FT, fibres.We can call these ST and FT muscles.Many muscles, however, contain a mixture of both types of fibre.People differ in the pattern of fibres in their muscles.For example, the proportion of ST fibres in the vastus lateralis muscle, measured in biopsies, has been found to vary from 10 to over 80 per cent (Grindrod, Round & Rutherford, 1987).It is generally considered that these patterns are genetically determined.

The relevance of this to the problem of adaptation is that ST fibres have a higher contraction coupling efficiency than FT fibres.In muscles contracting isometrically, so that no external work is done, ST muscles use less ATP per unit tension developed (Gibbs & Gibson, 1972; Wendt & Gibbs, 1973; Awan & Goldspink, 1972; Goldspink, 1975; Crow & Kushmerik, 1982).In isotonic contractions, where the muscle is allowed to shorten, the efficiency depends not only on the fibre type but also on the speed of shortening.When muscles of different species were compared an inverse relationship was found between intrinsic speed of shortening and biochemical efficiency (Nwoye & Goldspink, 1981).In the intact animal, as the rate of work increases, more and more FT fibres are recruited (Armstrong & Laughlin, 1985).One would expect this to be accompanied by a decrease in biochemical efficiency.

In man a positive correlation has been found between the percentage of ST fibres in the vastus lateralis muscle of the thigh and the force developed in an isometric contraction (Young, 1984; Grindrod et al., 1987).In what can only be described as a heroic experiment Suzuki (1979) identified two groups, each of three subjects; the ST group had 70-90 per cent of ST fibres in the vastus lateralis; the other group (FT) had only 15-30 per cent.Efficiency of work was measured as Δ work / Δ oxygen consumption on the bicycle ergometer.At 60 rpm there was no difference in efficiency between the two groups; at higher speeds the FT group was more efficient.It is a pity that in this experiment no tests were made at slower speeds and greater work loads.

In conditions of low energy intake and in hypothyroidism a reduction has been reported in the proportion and diameter of FT fibres (Russell et al., 1984; Wiles et al., 1979).In hypothyroidism this appears to be accompanied by an increase in the contraction coupling efficiency (Wiles et al., 1979; Leijendekker, van Hardeveld & Kassenaar, 1983).It is of interest in this connection that experimentally thyroidectomy has been found to cause a much greater depression of protein synthesis in the FT muscle gastrocnemius than in the ST soleus (Brown & Millward, 1983).Perhaps slow muscles and fibres are selectively preserved in conditions in which the metabolic rate is reduced.This would certainly make sense from the point of view of adaptation.


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